Peritumoral immune infiltrates in primary tumours are not associated with the presence of axillary lymph node metastasis in breast cancer: a retrospective cohort study

Author:

López Carlos12,Bosch-Príncep Ramón1,Orero Guifré1,Fontoura Balagueró Laia1,Korzynska Anna3,García-Rojo Marcial4,Bueno Gloria5,Fernández-Carrobles Maria del Milagro5,Roszkowiak Lukasz3,Callau Casanova Cristina1,Salvadó-Usach M. Teresa12,Jaén Martínez Joaquín1,Gibert-Ramos Albert1,Roso-Llorach Albert6,Gras Navarro Andrea1,Berenguer-Poblet Marta27,Llobera Montse8,Gil Garcia Júlia9,Tomás Bárbara1,Gestí Vanessa1,Laine Eeva7,Plancoulaine Benoít10,Baucells Jordi11,Lejeune Maryléne12

Affiliation:

1. Department of Pathology, Hospital de Tortosa Verge de la Cinta, Tortosa, Spain

2. Campus Terres de l’Ebre, Universitat Rovira Virgili Tarragona, Tortosa, Spain

3. Laboratory of Processing and Analysis of Microscopic Images, Nałęcz Institute of Biocybernetics and Biomedical Engineering, Warsaw, Poland

4. Department of Pathology, Hospital Universitario Puerta del Mar, Cádiz, Spain

5. VISILAB, Universidad de Castilla-La Mancha, Ciudad Real, Spain

6. Institut Universitari d’Investigació en Atenció Primària Jordi Gol, Barcelona, Spain

7. Department of Knowledge Management, Hospital de Tortosa Verge de la Cinta, Tortosa, Spain

8. Department of Oncology, Hospital de Tortosa Verge de la Cinta, Tortosa, Spain

9. Department of Surgery, Hospital Universitari de Girona Dr Josep Trueta, Girona, Spain

10. UNICAEN, INSERM, ANTICEPE, Université de Caen Basse Normandie, Caen, France

11. Department of Informatics, Hospital de Tortosa Verge de la Cinta, Tortosa, Spain

Abstract

Background The axillary lymph nodes (ALNs) in breast cancer patients are the body regions to where tumoral cells most often first disseminate. The tumour immune response is important for breast cancer patient outcome, and some studies have evaluated its involvement in ALN metastasis development. Most studies have focused on the intratumoral immune response, but very few have evaluated the peritumoral immune response. The aim of the present article is to evaluate the immune infiltrates of the peritumoral area and their association with the presence of ALN metastases. Methods The concentration of 11 immune markers in the peritumoral areas was studied in 149 patients diagnosed with invasive breast carcinoma of no special type (half of whom had ALN metastasis at diagnosis) using tissue microarrays, immunohistochemistry and digital image analysis procedures. The differences in the concentration of the immune response of peritumoral areas between patients diagnosed with and without metastasis in their ALNs were evaluated. A multivariate logistic regression model was developed to identify the clinical-pathological variables and the peritumoral immune markers independently associated with having or not having ALN metastases at diagnosis. Results No statistically significant differences were found in the concentrations of the 11 immune markers between patients diagnosed with or without ALN metastases. Patients with metastases in their ALNs had a higher histological grade, more lymphovascular and perineural invasion and larger-diameter tumours. The multivariate analysis, after validation by bootstrap simulation, revealed that only tumour diameter (OR = 1.04; 95% CI [1.00–1.07]; p = 0.026), lymphovascular invasion (OR = 25.42; 95% CI [9.57–67.55]; p < 0.001) and histological grades 2 (OR = 3.84; 95% CI [1.11–13.28]; p = 0.033) and 3 (OR = 5.18; 95% CI [1.40–19.17]; p = 0.014) were associated with the presence of ALN metastases at diagnosis. This study is one of the first to study the association of the peritumoral immune response with ALN metastasis. We did not find any association of peritumoral immune infiltrates with the presence of ALN metastasis. Nevertheless, this does not rule out the possibility that other peritumoral immune populations are associated with ALN metastasis. This matter needs to be examined in greater depth, broadening the types of peritumoral immune cells studied, and including new peritumoral areas, such as the germinal centres of the peritumoral tertiary lymphoid structures found in extensively infiltrated neoplastic lesions.

Funder

Institute of Health Carlos III

European Union ERDF funds

Project AIDPATH FP7-PEOPLE Project

Publisher

PeerJ

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology,General Medicine,General Neuroscience

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