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Clinical and Translational Oncology

, Volume 20, Issue 6, pp 687–694 | Cite as

Recommendations for the follow-up care of female breast cancer survivors: a guideline of the Spanish Society of Medical Oncology (SEOM), Spanish Society of General Medicine (SEMERGEN), Spanish Society for Family and Community Medicine (SEMFYC), Spanish Society for General and Family Physicians (SEMG), Spanish Society of Obstetrics and Gynecology (SEGO), Spanish Society of Radiation Oncology (SEOR), Spanish Society of Senology and Breast Pathology (SESPM), and Spanish Society of Cardiology (SEC)

  • A. Barnadas
  • M. Algara
  • O. Cordoba
  • A. Casas
  • M. Gonzalez
  • M. Marzo
  • A. Montero
  • M. Muñoz
  • A. Ruiz
  • F. Santolaya
  • T. Fernandez
Open Access
Special Article

Abstract

The increased incidence and decreased mortality of breast cancer have produced an increased number of breast cancer survivors. The type of sequelae and comorbidities that these patients present call for a collaborative follow-up by hospital-based specialized care and primary care. In this document, we present a guideline drafted and agreed among scientific societies whose members care for breast cancer survivors. The purpose of this guideline is to achieve the shared and coordinated follow-up of these patients by specialized care and primary care professionals. In it, we review the health issues derived from the treatments performed, with recommendations about the therapeutic approach to each of them, as well as a proposal for joint follow-up by primary and specialized care.

Keywords

Breast cancer Treatment chronic side effects sequelae Follow-up guidelines Primary care Specialized care 

Introduction

Breast cancer is the most common malignancy in the female population, with a cure rate that exceeds 80%. The gradual increase in incidence, associated with an aging population and the implementation of screening programs, together with lower mortality rates, account for an increased number of patients who are breast cancer survivors (BCSs) [1].

BCSs often have a life that is conditioned by the sequelae or morbidities related to treatment of the disease and, despite the high cure rates, many of the patients are no longer able to enjoy the quality of life achieved by women in our society. The treatments administered can leave physical, psychological, and psychosocial sequelae that may manifest or persist even years after having completed treatment and can interfere with their well-being and reincorporation into ordinary social and occupational activities [2].

Breast cancer is not a single disease, and treatment options depend on each tumor’s biology and behavior, as well as on each patient’s characteristics. Among patient characteristics, we must mention age, overall health status, and menopause status as being highly important factors when defining individualized treatment and preventing certain treatment-derived complications [3].

There are three essential aims that BCS follow-up pursues: (1) early diagnosis of relapses, (2) minimizing the impact of sequelae and complications derived from breast cancer diagnosis and treatment, and (3) encouraging healthcare and preventive measures to promote well-being and decrease risks to their health. Thus, a better quality of life might be achieved by helping BCSs to reintegrate as fully as possible into the various areas of their lives, i.e., family, work, and social activities [4, 5].

The need for specialized hospital-based care (SC) and primary care (PC) to share BCS patient follow-up activities has become evident in recent years and requires effective coordination. This shared, coordinated follow-up must ensure that the three previously named goals are met. The primary care physician plays a prominent role in detecting relapses and second neoplasms, dealing with late-onset effects of cancer treatment, managing comorbidity, psychological care, promoting healthy lifestyles, and recommending health prevention strategies, as well as normalizing the healthcare of patients who have been cured of breast cancer. Furthermore, BCSs continue to benefit from receiving care by the hospital-based specialist, especially during the first 5 years of follow-up [6, 7, 8, 9].

In this document, we present a guideline that has been drafted and agreed among different scientific societies whose members care for BCSs. The purpose of this guideline is to archive that the follow-up of these patients will be shared, collaborative, and coordinated among SC and PC professionals.

Treatment-derived health problems

As previously noted, the therapies administered may entail different sequelae that can translate into impaired quality of life for women who have overcome breast cancer. Some sequelae are late onset. Identifying these issues and correcting them can improve adaptation to daily life [9]. On the other hand, certain adverse effects may condition adherence to prolonged hormone therapy. It is also important to know whether the patients are receiving other medications or alternative therapies that might interfere with the activity of endocrine therapy. The PC physician is best suited to detect and control these side effects.

The side effects that call for special attention according to their frequency are as follows: lymphedema, effects derived from ovarian failure and menopause-related symptoms, overweight, cardiotoxicity, other vascular toxicities, neurotoxicity, ocular toxicity, cognitive impairment, skin alterations, and the risk of second neoplasms. The characteristics of these side effects and management recommendations are summarized in Table 1.
Table 1

Side effects and recommendations for their management

Side effect

Characteristics

Attitude/recommendation

Lymphedema

10–30% of patients who have undergone axillary node removal and 3–10% of patients treated with selective sentinel node biopsy [10]

In recent years, the strategy of substituting axillary lymphadenectomy for axillary radiation is being assessed, without losing effectiveness and with a decreased risk of lymphedema [12]

Preventive measures (hygiene, hydratation, avoiding weights, and wounds)

Rehabilitation

In some cases, lymphedema surgery may be considered

Ovarian failure and menopause-related symptoms

 Repercussions of ovarian function

20 and 80% of women may present amenorrhea secondary to chemotherapy, which may be permanent. The risk depends on the schedule administered and patient’s age at the time of chemotherapy administration

Offer fertility-preserving methods

Refer to Reproduction Services prior to systemic treatment administration [13]

Do not recommend conception until 3–6 months after completing systemic treatment [13, 14]

If the patient is receiving tamoxifen and wishes to become pregnant, hormone therapy must be discontinued between 3 and 6 months prior to allowing conception [13, 15]

 Sexual activity

Decrease in libido or vaginal dryness are attributable to both the ovarian failure young women undergo after chemotherapy or hormone therapy and the side effects themselves of hormone therapy (gonadotropin analogues, SERM, aromatase inhibitors)

The change in body image and local pain secondary to surgery can also cause dysfunction of sexual activity

Psychological support

Use of vaginal lubricants

The use of vaginal tablets or hormone creams is controversial

 Hot flashes secondary to menopause

They are the result of induced menopause and are aggravated by hormone treatments

Both tamoxifen and aromatase inhibitors (anastrozole, letrozole, exemestane) can cause or aggravate hot flashes

If severe, treatment with velafaxine or gabapentin can be used

Acupuncture has demonstrated efficacy

 Risk of endometrial disease

Women who receive tamoxifen for a long period have a higher risk of suffering endometrial cancer, although these neoplasms are general diagnosed very early have a good prognosis

In patients receiving tamoxifen, annual gynecological examinations are recommended. Postmenopausal women should be evaluated preferably by a gynecologist if they present vaginal bleeding

 Bone health

Spontaneous or induced menopause (secondary to chemotherapy, gonadotropin analogues, or oophorectomy) involves decreased bone mineral density

This effect can be relevant in young women with early menopause

Hormone treatment, especially aromatase inhibitors in postmenopausal women produce a faster decline in bone mineral density with an increased risk of osteoporotic fractures

In menopausal patients, a baseline densitometry is recommended when starting endocrine therapy. Depending on the results, patients should be referred to a Bone Metabolism Service or follow ASCO/ESMO recommendations [16, 17]. Patients who are given aromatase inhibitors should receive calcium and vitamin D supplements. If osteoporosis is detected, add bone resorption inhibitors

Recommend aerobic exercise

Quit smoking

 Joint pain

This is a very common side effect, particularly in patients treated with aromatase inhibitors

Increase frequency and duration of physical exercise

Minor analgesics

Acupuncture can be beneficial

 Limited mobility of the scapulohumeral joint on the same side as the breast lesion

One side effect that can present long term following axillary radiation is decreased mobility of the scapulohumeral joint on the side that received radiation secondary to fibrosis in the pectoral muscle of the side affected [18]

Moderate, but constant physical exercise in the limb that received radiation

On occasion, if improvement is not seen, the help of Rehabilitation Specialists should be requested

Overweight

Weight gain is common during treatment for breast cancer, especially in women in whom menopause is induced or who follow hormone deprivation treatment

Furthermore, overweight has been recognized, not only as a risk factor for breast cancer but also as an unfavorable factor for relapse [19]

Monitor and control weight

Low calorie diets

Physical exercise (150 min/week)

Psychological support

Cardiotoxicity and other vascular toxicities

Control concomitant diseases (hypertension, diabetes, obesity)

Promotion of healthy lifestyles

Refer to cardiology if signs of heart failure appear

Yearly incidence of ventricular dysfunction of approximately 9% that exceeds 40% in patients over the age of 75 years or having prior heart disease

Toxicity due to anthracyclines is sometimes detected late and is more serious and often irreversible compared to toxicity due to trastuzumab [20], which tends to be reversible

Toxicity secondary to anthracyclines is unusual if cumulative doses of 250 mg/m2 of adriamycin or 550 mg/m2 of epirubicin [3, 21] are not exceeded

 

Cardiotoxicity due to trastuzumab usually appears during the active treatment phase and indicates that treatment must be withdrawn, although a high percentage of cases recover without sequelae. In women who have presented heart failure, there is no complete evidence as to whether it is possible to discontinue long-term cardiological treatment [22, 23, 24]

Deep-vein thrombosis (DVT) or pulmonary thromboembolism can be a side effect of tamoxifen and, less often, of aromatase inhibitors

If deep-vein thrombosis develops, refer patient to the oncologist to evaluate the advisability of continuing endocrine treatment

In patients who have received complementary radiation therapy, especially in the case of tumors on the left side and when the internal mammary chain has been radiated, long-term follow up must be carried out, given the risk of late cardiac toxicity. Nevertheless, the more modern radiation techniques with three-dimensional planning and dose intensity modulation have made it possible to lower the incidence of this type of side effect [25, 26], although risk factors should be strictly controlled and the advisability of stress testing should be assessed [15]

 

Neurotoxicity

This is a side effect associated with the administration of taxanes. Sensory neurotoxicity in the form of paresthesia and pain in the hands and feet causes great discomfort

Detect toxicity early

There is no specific treatment

Duloxetine, gabapentin, and pregabalin can improve symptoms

 Ocular toxicity

Though uncommon, tamoxifen can increase the risk of cataracts

Refer to ophthalmologist if symptoms of blurry vision appear

Asthenia

Asthenia is a highly prevalent symptom in breast cancer that often persists after competing treatments [27]

The use of a visual numeric scale is recommended to quantify the degree of asthenia and should be monitored

Rule out organic cause

Psychoemotional support

Physical activity

Cognitive impairment

Although there are few studies, many patients report memory loss or losing the ability to concentrate after chemotherapy that can last more than 20 years after treatment

Methods are being investigated that enable us to diagnose and follow-up on this side effect

Assessment by Neurology

Concentration and visual memory exercises

Reading

Skin changes (dryness, alopecia, others)

Following treatment with chemotherapy, some women do not recover all their hair or present side effects of the skin and related structures, such as the nails

Evaluation by Dermatologist

Risk of second neoplasms

Patients who have undergone radiation therapy are at increased risk for a second neoplasm related to treatment with radiation. This phenomenon usually occurs many years after having received radiotherapy. The tumors that appear most often are neoplasms of the lung or angiosarcomas of the chest wall [28, 29]

Factors related to lung cancer should be avoided, especially with respect to smoking

In addition, there are general recommendations that must be followed [8, 9]:
  • Overweight avoidance Weight gain has been associated with a worse treatment response and greater risk of relapse.

  • Healthy diet and exercise Epidemiological studies have proven a benefit for patients following a low-fat diet together with at least 150 min of vigorous physical activity per week [10]. The recommended diet is high in fresh fruits, vegetables, and legumes (at least two pieces of fruit per day); patients are also recommended to lower their intake of red meat (to 1–2 times per week) and processed meats and increase consumption of blue fish, olive oil use and consume dairy products, as well as take advantage of all the elements comprising a Mediterranean diet.

  • Smoking avoidance

  • Moderate alcohol intake It is recommended that women abstain from drinking more than 20 g of alcohol per day. The following beverages equal 20 g of alcohol: 250 ml of beer, one glass of red wine (150 ml), or a quarter of a glass (25 ml) of a higher grade liquor (e.g., gin, whisky, anise, and tequila).

  • Use of complementary therapies Some of these therapies could interfere with patient treatment. Acupuncture must be properly performed and with necessary aseptic measures to minimize the risk of infection. Complementary or integrative therapies cannot substitute for a specific antitumor treatment.

  • Awareness of symptoms that indicate possible relapse or second tumors The following symptoms should be monitored: persistent bone pain that increases with movement and fails to remit with rest, persistent cough, dyspnea, asthenia, anorexia, or unexplained weight loss, vaginal bleeding in postmenopausal women, change in intestinal rhythm, rectal bleeding, or persistent headache or other neurological deficit. Thus, an early diagnosis can be made.

  • Confirmation of compliance with antiestrogenic hormone therapy Control and positive reinforcement to maintain the prescribed treatment even over prolonged periods (5–10 years).

  • Return to work Support and guidance appropriate to the patient’s stage of evolution. In the case of complementary treatment, it is recommended that patients wait for a reasonable time so that they can recover from the side effects of treatment.

  • Active alertness of the appearance of symptoms suggestive of heart disease.

Proposal of joint primary care and specialized care follow-up (Table 2)

Studies conducted thus far have revealed that radiological testing is not useful, except for yearly mammograms and that a PC physician or nurse can conduct follow-up if they are motivated and trained to care for the complications or morbidities that BCS present. Patient satisfaction will depend more on how they are treated than on where follow-up is undertaken. Studies have also concluded that relapses are detected similarly in PC or SC and that there are no differences in overall survival with any of the different follow-up schemes (with imaging studies and tumor markers compared with history, breast examination, and yearly mammogram), if the patient is guaranteed access to healthcare services in the presence of a symptom or sign of alarm [11].
Table 2

Proposed follow-up together with primary care

Risk group

Definition

Recommendation

Low risk

Hormone-sensitive tumor

Size ≤ 2 cm (category pT1)

No axillary metastases

Low risk according to genomic platform

Carcinoma “in situ”

Clinical check-up every 6 months, alternating with primary care (PC) for 5 years

After 5 years, only PC will be responsible for check-ups

Yearly mammogram

Intermediate risk

Hormone-sensitive tumor

Size between 2 and 5 cm (category pT2)

No nodal metastases or axillary metastases involving between 1 and 3 nodes

Intermediate risk according to genomic platform

Check-up every 4 months together with PC for the first 2 years

Every 6 months until the fifth year

Only PC will be responsible for check-ups after that

Yearly mammogram

High risk

Tumor not expressing hormone receptors

Tumor with HER2 amplification

High risk tumor according to genomic platform

Tumor with metastases in more than 3 axillary nodes

Tumor treated with neoadjuvant therapy

Locally advanced tumor

Check-up every 4 months together with PC for 5 years

After 5 years, every 6 months together with PC until 10 years

Only PC will be responsible for check-ups after that

Yearly mammogram

At every visit, the following should be performed: (i) Complete anamnesis evaluating the presence of comorbidities. (ii) Evaluation of hormone treatment compliance (whenever prescribed). (iii) Detection of side effects. (iv) Physical examination of the mammary glands, rib cage, or area of breast reconstruction and lymph node chain. (v) Foster a healthy lifestyle

However, long-term survivors who have overcome breast cancer require outstanding coordination and communication between PC and SC. It is proposed that patients already treated in the hospital be classified into three groups: (1) low risk; (2) intermediate risk, and (3) high risk. Table 2 summarizes the management recommendations coordinated between PC and SC.

Follow-up visits of female BCSs should include the following:
  • History aimed at ruling out warning signs of relapse or the presence of sequelae, comorbidities, or second neoplasms.

  • Adherence to adjuvant endocrine therapy when indicated.

  • A physical examination that includes examination of the breasts and adjacent node regions.

  • Bilateral, yearly mammograms in two projections, after conservative surgery of the breast or if the breast has been reconstructed. Annual follow-up visits will be maintained throughout their lifetime because these patients, unlike the healthy population who undergo biannual mammograms in screening campaigns, have a 5–10% probability of developing local relapse or a second neoplasm within 10 years post-treatment; this higher risk remains throughout their entire lives. Mammograms can be performed within the scope of PC or with the aid of the specialist in Obstetrics and Gynecology.

  • Recommendations for prevention and health promotion.

Role of the primary care physician

More and more women who have had breast cancer are being cared for in primary care. Optimal care by the PC physician includes the prevention, detection of relapses and possible second neoplasms, care for comorbidities, and the approach to late-onset effects of cancer treatment. It is also up to the PC physician to refer all women who have had breast cancer and present an accumulation of cases of cancer in the family to the reference Genetic Counseling Centers. The criteria for reference to a Genetic Counseling Center are as follows: having one or more first- or second-degree relatives with a breast or ovarian tumor under the age of 50; having a relative with bilateral breast tumors, having a male relative with breast cancer; having a relative with breast cancer with a triple-negative phenotype and less than 60 years of age [10]. Patients should also be referred to these centers when colon cancer is detected in different members of the family under the age of 50 at presentation.

Follow-up of BCS calls for a multidisciplinary approach and excellent coordination and communication between PC and SC. The oncologist should facilitate a case report when initiating and completing treatment; this report should include the type and clinical status of the tumor, treatment intent, treatments received, and toxicities that may have arisen during treatment. This information is fundamental to elaborating an individualized care plan that makes appropriate follow-up possible.

Below is the proposed minimum content that would be advisable to include in the report issued by SC to share patient information with PC:

Initial oncological report

  1. 1.

    Disease debut (symptom duration, origin [population screening programs, fast track diagnostics, PC physician, others]).

     
  2. 2.

    Diagnostic testing (imaging studies performed to determine the diagnosis, pathology results of biopsy with immunohistochemical report, clinical TNM).

     
  3. 3.

    Surgical procedure (if performed, and postoperative TNM).

     
  4. 4.

    Extension study, prognostic and predictive factors, results of the genomic study of the risk of relapse (if performed).

     
  5. 5.
    General treatment approach and anticipated date of initiation Medical Oncology’s treatment prescription:
    1. (a)

      Drugs

       
    2. (b)

      Sequence of administration. Courses

       
    3. (c)

      Anticipated duration.

       
     
  6. 6.
    Radiation treatment approach (when applicable):
    1. (a)

      Volumes to be treated, total dose, and fractioning.

       
    2. (b)

      Radiotherapy technique: 3D, IMRT, partial radiation, intraoperative radiation, source, and energy.

       
    3. 7.

      Prevention guidelines considering possible side effects of treatment.

       
    4. 8.

      Report if patient is participating in a Clinical Trial.

       
    5. 9.

      Estimation of time off work Consideration must be paid as to whether the time off work has to do with the characteristics of the workplace, associated risks, and compatibility with the degree of functioning following treatment.

       
    6. 10.

      Date of the next visit to SC. In some Autonomous Communities, the PC physician can consult them, but not in all of them.

       
     

Report upon completion of the initial phase of treatment

Once the initial stage of treatment is completed (surgery, treatment with chemotherapy, and/or targeted drugs and radiotherapy), after the first 6–15 months, a new stage opens. This period is no less important than the diagnostic stage, given the uncertainty surrounding the quality and continuity of life, during which information about the patient’s status must be shared again with PC physicians.
  1. 1.
    Regarding clinical situation during the initial stage of treatment.
    1. (a)

      Full report that includes the previously listed items (points 1, 2, 3, and 4);

       
    2. (b)

      All treatments received: radiotherapy, hormone therapy, or biological therapy, and if the patient has been included in a clinical trial. Treatment duration and related side effects and their treatment prevention (points 5 and 6);

       
    3. (c)

      Information about the risk of cardiotoxicity and type of cardiovascular monitoring undertaken;

       
    4. (d)

      Overall evolution;

       
    5. (e)

      Information regarding schedules for follow-up: tests and timing, outline of visits with SC.

       
     
  2. 2.
    Regarding clinical recommendations
    1. (a)

      Warning signs that a new appointment should be set up with SC;

       
    2. (b)

      Specific approach to lymphedema: when, how, and who to refer to;

       
    3. (c)

      Motor rehabilitation if necessary and recommendations regarding physical exercise;

       
    4. (d)

      Specific approach toward side effects of hormone medication. Recommendations for the prevention/treatment of osteoporosis and related side effects;

       
    5. (e)

      Control of mammary implants/expander/prosthetic replacement, and related events;

       
    6. (f)

      Dietary recommendations;

       
    7. (g)

      Special considerations regarding patients’ health issues and comorbidities, and

       
    8. (h)

      Complementary therapies and their repercussions.

       
     
  3. 3.
    Psychosocial and occupational recommendations
    1. (a)

      Specific aspects to be considered depending on the patient’s psychological situation, family and social impact. Need for specific social support;

       
    2. (b)

      Psychological approach. Fear of relapse;

       
    3. (c)

      Recommendations about sexuality and contraception;

       
    4. (d)

      Recommendations about returning to work or resuming previous activities. Pursuing a life path/professional plan, and

       
    5. (e)

      In certain women who want to be mothers, recommendations will be made about the best time to conceive. Young women who have preserved oocytes or ovarian cortex should be referred to Fertility Services at the Obstetrics and Gynecology Department.

       
     

Notes

Acknowledgements

The authors would like to thank Fernando Rico-Villademoros (COCIENTE SL, Madrid, Spain) for editorial assistance in the preparation of this manuscript.

Compliance with ethical standards

Funding

This work has not received any funding.

Conflict of interest

The authors declare no conflict of interest regarding this manuscript.

Research involving human participants and/or animals

The manuscript does not contain clinical studies or patient data.

Informed consent

Not applicable.

References

  1. 1.
    Rojas MP, Telaro E, Russo A, Moschetti I, Coe L, Fossati R, et al. Follow up strategies for women treated for early breast cancer. Cochrane Database Sys Rev. 2005;25:CD001768.Google Scholar
  2. 2.
    National Institute for Clinical Excellence (2002). Guidance on Cancer Services: improving outcomes in breast cancer. Manual update. London: National Institute for Clinical Excellence. http://www.nice.org.uk/guidance/csgbc/evidence/improving-outcomes-in-breast-cancer-manual-update-2.
  3. 3.
    Merck B, Vicente F, Clínico en Cáncer de Mama S. Manual de Práctica Clínica en Senología 2012. 2nd ed. Madrid: Fundación Española de Senología y Patología Mamaria; 2012. pp. 119–20.Google Scholar
  4. 4.
    Tellez de Peralta FJ. Seguimiento y control del cáncer de mama operado. In: Guías Clínicas de la Asociación Española de Cirujanos, Cirugía de la mama. Madrid: Ediciones Arán; 2006. pp. 326–333.Google Scholar
  5. 5.
    Khatcheressian JL, Hurley P, Bantug E, Esserman LJ, Grunfeld E, Halberg F, et al. Breast cancer follow-up and management after primary treatment: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2013;31:961–5. doi: 10.1200/JCO.2012.45.9859.CrossRefPubMedGoogle Scholar
  6. 6.
    Arbona Rovira A, Martínez Lorenzo M, Fierro Barrabés G, Aguinaga Aizcorreta Ma T. Enfermería Oncológica. Unidad de Mama. Hospital de Día. Investigación Oncológica. Manual de Práctica Clínica en Senología 2012. 2nd ed. Madrid: Fundación Española de Senología y Patología Mamaria; 2012. pp. 120–123.Google Scholar
  7. 7.
    Ferro T, Prades J. Necesidades de información en el cáncer de mama y de atención en la supervivencia. 1st ed. Barcelona: Federación Española de Cáncer de mama; 2013. http://fecma.vinagrero.es/documentos/LIBRONEC.pdf.
  8. 8.
    Feliu J, Virizuela JA. El seguimiento en los supervivientes de cáncer: una responsabilidad compartida. Med Clín. 2011;137:163–5. doi: 10.1016/j.medcli.2011.03.016.CrossRefGoogle Scholar
  9. 9.
    Plan integral de atención a los largos supervivientes de cáncer. Sociedad Española de Oncología. Médica (SEOM). Madrid: Zentrum Verlagsgesellschaft.; 2013, pp 77–82.Google Scholar
  10. 10.
    Hidding JT, Beurskens CH, van der Wees PJ, van Laarhoven HW, Nijhuis-vander Sanden MW. Treatment related impairments in arm and shoulder in patients with breast cancer: a systematic review. PLoS One. 2014;9:e96748. doi: 10.1371/journal.pone.0096748.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Grunfeld E, Julian JA, Pond G, Maunsell E, Coyle D, Folkes A, et al. Evaluating survivorship care plans: results of a randomized, clinical trial of patients with breast cancer. J Clin Oncol. 2011;29:4755–62. doi: 10.1200/JCO.2011.36.8373.CrossRefPubMedGoogle Scholar
  12. 12.
    Donker M, van Tienhoven G, Straver ME, Meijnen P, van de Velde CJ, Mansel RE, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol. 2014;15:1303–10. doi: 10.1016/S1470-2045(14)70460-7.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Loren AW, Mangu PB, Beck LN, Brennan L, Magdalinski AJ, Partridge AH, et al. Fertility preservation for patients with cancer: American Society of Clinical Oncology clinical practice guideline update. J Clin Oncol. 2013;31:2500–10. doi: 10.1200/JCO.2013.49.2678.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Azim HA, Davidson NE, Ruddy KJ. Challenges in treating premenopausal women with endocrine-sensitive breast cancer. Am Soc Clin Oncol Educ Book. 2016;35:23–32. doi: 10.14694/EDBK_159069.CrossRefPubMedGoogle Scholar
  15. 15.
    Braems G, Denys H, De Wever O, Cocquyt V, Van den Broecke R. Use of tamoxifen before and during pregnancy. Oncologist. 2011;16:1547–51. doi: 10.1634/theoncologist.2011-0121.CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Runowicz CD, Leach CR, Henry NL, Henry KS, Mackey HT, Cowens-Alvarado RL, et al. Recommendations for the follow-up care of female breast cancer survivors. J Clin Oncol. 2016;34:611–35. doi: 10.1200/JCO.2015.64.3809.CrossRefPubMedGoogle Scholar
  17. 17.
    Coleman R, Body JJ, Aapro M, Hadji P, Herrstedt J, ESMO Guidelines Working Group. Bone health in cancer patients: ESMO clinical practice guidelines. Ann Oncol. 2014;25(Suppl 3):iii124–37. doi: 10.1093/annonc/mdu103.CrossRefPubMedGoogle Scholar
  18. 18.
    Bentzen SM, Dische S. Morbidity related to axillary irradiation in the treatment of breast cancer. Acta Oncol. 2000;39:337–47. doi: 10.1080/028418600750013113.CrossRefPubMedGoogle Scholar
  19. 19.
    Chlebowski RT, Blackburn GL, Thomson CA, Nixon DW, Shapiro A, Hoy MK, et al. Dietary fat reduction and breast cancer outcome: interim efficacy results from the Women’s Intervention Nutrition Study. J Natl Cancer Inst. 2006;98:1767–76. doi: 10.1093/jnci/djj494.CrossRefPubMedGoogle Scholar
  20. 20.
    Ewer MS, Vooletich MT, Durand JB, Woods ML, Davis JR, Valero V, et al. Reversibility of trastuzumab-related cardiotoxicity: new insights based on clinical course and response to medical treatment. J Clin Oncol. 2005;23:7820–6. doi: 10.1200/JCO.2005.13.300.CrossRefPubMedGoogle Scholar
  21. 21.
    Cardinale D, Colombo A, Bacchiani G, Tedeschi I, Meroni CA, Veglia F, et al. Early detection of anthracycline cardiotoxicity and improvement with heart failure therapy. Circulation. 2015;131:1981–8. doi: 10.1161/CIRCULATIONAHA.114.013777.CrossRefPubMedGoogle Scholar
  22. 22.
    Cardinale D, Biasillo G, Cipolla CM. Curing cancer, saving the heart: a challenge that cardioncology should not miss. Curr Cardiol Rep. 2016;18:51. doi: 10.1007/s11886-016-0731-z.CrossRefPubMedGoogle Scholar
  23. 23.
    Curigliano G, Cardinale D, Dent S, Criscitiello C, Aseyev O, Lenihan D, et al. Cardiotoxicity of anticancer treatments: epidemiology, detection, and management. CA Cancer J Clin. 2016;66:309–25. doi: 10.3322/caac.21341.CrossRefPubMedGoogle Scholar
  24. 24.
    Zamorano JL, Lancellotti P, Rodriguez Muñoz D, Aboyans V, Asteggiano R, Galderisi M, et al. 2016 ESC Position Paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for Practice Guidelines: the Task Force for Cancer Treatments and Cardiovascular Toxicity of the European Society of Cardiology (ESC). Eur Heart J. 2016;37:2768–801. doi: 10.1093/eurheartj/ehw211.CrossRefPubMedGoogle Scholar
  25. 25.
    Jagsi R, Griffith KA, Koelling T, Roberts R, Pierce LJ. Rates of myocardial infarction and coronary artery disease and risk factors in patients treated with radiation therapy for early-stage breast cancer. Cancer. 2007;109:650–7. doi: 10.1002/cncr.22452.CrossRefPubMedGoogle Scholar
  26. 26.
    Darby SC, Ewertz M, McGale P, Bennet AM, Blom-Goldman U, Brønnum D, et al. Risk of ischemic heart disease in women after radiotherapy for breast cáncer. N Engl J Med. 2013;368:987–98. doi: 10.1056/NEJMoa1209825.CrossRefPubMedGoogle Scholar
  27. 27.
    Bower JE, Bak K, Berger A, Breitbart W, Escalante CP, Ganz PA, et al. Screening, assessment, and management of fatigue in adult survivors of cancer: an American Society of Clinical Oncology clinical practice guideline adaptation. J Clin Oncol. 2014;32:1840–50. doi: 10.1200/JCO.2013.53.4495.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Deutsch M, Land SR, Begovic M, Wieand HS, Wolmark N, Fisher B. The incidence of lung carcinoma after surgery for breast carcinoma with and without postoperative radiotherapy. Results of National Surgical Adjuvant Breast and Bowel Project (NSABP) clinical trials B-04 and B-06. Cancer. 2003;98:1362–8. doi: 10.1002/cncr.11655.CrossRefPubMedGoogle Scholar
  29. 29.
    Karlsson P, Holmberg E, Samuelsson A, Johansson KA, Wallgren A. Soft tissue sarcoma after treatment for breast cancer–a Swedish population-based study. Eur J Cancer. 1998;34:2068–75. doi: 10.1016/S0959-8049(98)00319-0.CrossRefPubMedGoogle Scholar

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© The Author(s) 2017

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Department of Medical OncologyHospital de la Santa Cruz y San PabloBarcelonaSpain
  2. 2.Department of Radio-oncologyParc de Salut MarBarcelonaSpain
  3. 3.Department of Gynecology and ObstetricsHospital de la Vall d’HebrónBarcelonaSpain
  4. 4.Department of Medical OncologyHospital Virgen del RocíoSevilleSpain
  5. 5.Montesa Healthcare Center, Servicio Madrileño de SaludMadridSpain
  6. 6.Catalonian Health InstituteBarcelonaSpain
  7. 7.Department of Radio-oncologyHospital Universitario HM SanchinarroMadridSpain
  8. 8.Department of Medical OncologyHospital Clínic BarcelonaBarcelonaSpain
  9. 9.Department of Medical OncologyInstituto Valenciano de OncologíaValenciaSpain
  10. 10.Ciudad San Pablo Healthcare Center, Servicio Madrileño de SaludMadridSpain
  11. 11.Department of CardiologyHospital La Paz MadridMadridSpain

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