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Sentinel Lymph Node Biopsy in Breast Cancer-Aspects on Indications and Limitations

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Sentinel Lymph Node Biopsy in Breast Cancer-Aspects on Indications and Limitations From the Department of Clinical Science and Education, Södersjukhuset Karolinska Institutet, Stockholm, Sweden SENTINEL LYMPH NODE BIOPSY IN BREAST CANCER-ASPECTS ON INDICATIONS AND LIMITATIONS Linda Holmstrand Zetterlund Stockholm 2017 Front page illustration: Reproduced with permission from IntraMedical Imaging LLC. All previously published papers were reproduced with permission from the publisher. Published by Karolinska Institutet. Printed by E-Print AB 2017. © Linda Zetterlund, 2017 ISBN 978-91-7676-576-0 Institutionen för klinisk forskning och utbildning Sentinel lymph node biopsy in breast cancer – Aspects on indications and limitations AKADEMISK AVHANDLING som för avläggande av medicine doktorsexamen vid Karolinska Institutet offentligen försvaras i Aulan, Södersjukhuset. Fredagen den 21 april, kl 09.00 av Linda Holmstrand Zetterlund Huvudhandledare: Fakultetsopponent: MD PhD Fuat Celebioglu Ellen Schlichting, MD, PhD Karolinska Institutet Oslo Universitet Institutionen för klinisk forskning Institutt for klinisk medisin, Medicinsk fakultet och utbildning Bihandledare: Betygsnämnd: Professor Rimma Axelsson Docent Signe Borgquist Karolinska Institutet Lunds Universitet Institutionen för klinisk vetenskap, Institutionen för kliniska vetenskaper, intervention och teknik Avdelningen för onkologi och patologi Docent Jana de Boniface Karolinska Institutet Docent Jan Zedenius Institutionen för molekylär medicin Karolinska Institutet och kirurgi Institutionen för molekylär medicin och kirurgi Professor Jan Frisell Karolinska Institutet Johan Lindholm Institutionen för molekylär medicin Karolinska Institutet och kirurgi Institutionen för onkologi och patologi Stockholm 2017 Till Fredrik, Klara och Hugo ABSTRACT __________________________________________________________________________ Axillary lymph node status is the most important prognostic factor in breast cancer. Sentinel lymph node biopsy (SLNB) was introduced in the late 1990s and has replaced axillary lymph node dissection (ALND) as the gold standard axillary nodal staging procedure in early breast cancer due to higher accuracy and less morbidity compared with ALND. The overall aim of this thesis was to investigate SLNB and its current role in breast cancer today with a focus on current controversies and its limitations in different clinical settings. The first paper (I) is a national registry study investigating the incidence of positive sentinel lymph nodes (SLNs) in women with a postoperative diagnosis of pure DCIS (ductal carcinoma in situ). We also investigated whether additional tumor sectioning could reveal occult tumor invasion among the patients with tumor deposits in their SLNs. SLNB was performed in 753 patients of whom 11 had tumor deposits in their SLNs. Two patients had macro- and three micrometastasis (N1). Six patients had isolated tumor cells (N0(i+)), resulting in a SLN positive rate of 0.7% (5/753). We did not find any risk factors for SLN metastasis. Occult invasion was found to the same extent among patients with SLN metastasis 9% (1/11) as in the matched control group of 10% (2/21). The aim of the second paper (II) was to evaluate lymph drainage patterns to the axillary lymph nodes with hybrid SPECT/CT imaging before, compared with six weeks after a diagnostic breast excision of an unsuspicious breast tumor. SPECT (single photon emission computed tomography) integrates nuclear medicine imaging with CT (computed tomography) which results in functional images with precise anatomical localization of radioactive SLNs. The contralateral breast served as a control. The SLN detection rate was 91.9% (34/37) on operated sides postoperatively compared with 93.7% (104/111) on non-operated sides, p=0.0771. Partial or total concordance regarding number and localization of radioactive lymph nodes was not significantly lower on operated at 85.7% (30/35) compared with 88.9% (32/36) on non-operated sides, P=0.735. In the third (III) and fourth (IV) papers SLNB in the neoadjuvant settting was evaluated in a Swedish prospective multicenter trial recruiting women with biopsy-verified breast cancer planned for neoadjuvant systemic therapy (NAST). In paper III clinically node-negative (cN0) patients were enrolled and SLNB performed prior to commencement of NAST. A completion ALND was performed in all patients in both trial arms. The identification rate (IR) was 100% (224/224). The proportion of patients with a negative SLNB but still positive lymph nodes in the axilla after NAST was 7.4% (9/121, 95%, CI: 4.0-13.5). In paper IV, SLNB was attempted after NAST in 195 patients with biopsy-proven node-positive breast cancer at stage T1-4d. The overall IR was 77.9% (152/195) and the overall FNR 14.1 % (13/92). The FNR decreased to 4.0% when two or more SLNs were retrieved. Conclusions: Positive SLNs are rare in pure DCIS. SLNB should only be performed if mastectomy is planned or in case of high risk of invasive disease if breast-conserving surgery is planned. SLNB after prior diagnostic surgery seems accurate with minor impact on lymph drainage patterns. SLNB in cN0 patients before NAST is highly reliable. SLNB after NAST in clinically node-positive patients with T1-4d stage breast cancer is feasible but associated with lower IR and higher FNR than in clinically node-negative patients. Only if two or more SLNs are retrieved can the omission of ALND be considered. LIST OF PUBLICATIONS __________________________________________________________________________ I. Zetterlund L, Stemme S, Arnrup H, de Boniface J. Incidence of and risk factors for sentinel lymph node metastasis in patients with a postoperative diagnosis of ductal carcinoma in situ Br J Surg. 2014; 101: 488-494 II. Zetterlun d L, Gabrielson S, Axelsson R, De Boniface J, Frisell J, Olsson A, Celebioglu F. Impact of previous surgery on sentinel lymph node mapping: hybrid SPECT/CT before and after a unilateral diagnostic breast excision The Breast 30 2016; 30: 32-38 III. Zetterlund L, Celebioglu F, Axelsson R, de Boniface J, Frisell J. Swedish prospective multicenter trial on the accuracy and clinical relevance of sentinel lymph node biopsy before neoadjuvant systemic therapy in breast cancer Breast Cancer Res Treat. Published on line: 17 Feb 2017 IV. Zetterlund LH, Frisell J, Zouzos A, Axelsson R, Hatschek T, de Boniface J, Celebioglu F. Swedish prospective multicenter trial evaluating sentinel lymph node biopsy after neoadjuvant systemic therapy in clinically node-positive breast cancer Breast Cancer Res Treat. Published on line: 21 Feb 2017 LIST OF ABBREVIATIONS __________________________________________________________________________ AJCC American Joint Committee on Cancer ALH Atypical lobular hyperplasia ALND Axillary lymph node dissection AUS Axillary ultrasound BCS Breast-conserving surgery CT Computed tomography DCIS Ductal carcinoma in situ DFS Disease-free survival ER Estrogen receptor FNAC Fine needle aspiration cytology FNR False negative rate HER2 Human epidermal growth factor receptor 2 HRT Hormone replacement therapy IBC Inflammatory breast cancer IHC Immunohistochemical IR Identification rate ITC Isolated tumor cells HER2 Human epidermal growth factor receptor 2 LABC Locally advanced breast cancer LCIS Lobular carcinoma in situ LN Lobular neoplasia MRI Magnetic resonance imaging NAC Neoadjuvant chemotherapy NAST Neoadjuvant systemic therapy NPV Negative predictive value PCR Pathological Complete Response NST No special type PET Positron emission tomography PLCIS Pleomorphic lobular carcinoma in situ PPV Positive predictive value PgR Progesteron receptor RCB Residual cancer burden SLN Sentinel lymph node SLNB Sentinel lymph node biopsy SPECT Single photon emission computed tomography SPIO Supraparamagnetic iron oxide TNM Tumor, node and metastasis CONTENTS __________________________________________________________________________ 1 Introduction ..................................................................................................................... 1 2 Background...................................................................................................................... 3 2.1 Anatomy of the breast ........................................................................................... 3 2.1.1 The lymphatic system ............................................................................... 3 2.2 Epidemiology and risk factors for breast cancer .................................................. 5 2.3 Tumor Classification ............................................................................................. 6 2.3.1 TNM classification .................................................................................... 6 2.3.2 Histological grade ..................................................................................... 7 2.3.3 Histopathologic type ................................................................................. 7 2.3.4 Biomarkers ................................................................................................ 9 2.3.5 Molecular subtypes ................................................................................. 10 2.4 Diagnosis ............................................................................................................. 10 2.5 Breast surgery ...................................................................................................... 11 2.6 Axillary surgery ................................................................................................... 12 2.6.1 Axillary lymph node dissection
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