Citation: Galiandro, F.; Agnes, S.;
Moschetta, G.; Orlandi, A.; Clarke, G.;
Bria, E.; Franceschini, G.; Treglia, G.;
Giovinazzo, F. Prognostic Factors in
Patients with Breast Cancer Liver
Metastases Undergoing Liver
Resection: Systematic Review and
Meta-Analysis. Cancers 2022, 14, 1691.
https://doi.org/10.3390/
cancers14071691
Academic Editor: Adam E. Frampton
Received: 3 February 2022
Accepted: 23 March 2022
Published: 26 March 2022
Publisher’s Note: MDPI stays neutral
with regard to jurisdictional claims in
published maps and institutional affil-
iations.
Copyright: © 2022 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
cancers
Systematic Review
Prognostic Factors in Patients with Breast Cancer Liver
Metastases Undergoing Liver Resection: Systematic Review and
Meta-Analysis
Federica Galiandro
1
, Salvatore Agnes
1
, Giovanni Moschetta
1
, Armando Orlandi
2
, George Clarke
3
,
Emilio Bria
2
, Gianluca Franceschini
4
, Giorgio Treglia
5,6,7,
* and Francesco Giovinazzo
1,
*
1
General Surgery and Liver Transplantation Unit, Fondazione Policlinico Universitario Agostino Gemelli,
00168 Rome, Italy; federica.galiandro@policlinicogemelli.it (F.G.); salvatore.agnes@policlinicogemelli.it (S.A.);
dott.moschetta@gmail.com (G.M.)
2
Oncology Unit, Fondazione Policlinico Universitario Agostino Gemelli, 00168 Rome, Italy;
armando.orlandi@policlinicogemelli.it (A.O.); emilio.bria@policlinicogemelli.it (E.B.)
3
Department of Liver Surgery, Queen Elizabeth Hospital, Birmingham B15 2GW, UK;
george.clarke@uhb.nhs.uk
4
Breast Unit, Fondazione Policlinico Universitario Agostino Gemelli, 00168 Rome, Italy;
gianluca.franceschini@policlinicogemelli.it
5
Academic Education, Research and Innovation Area, General Directorate, Ente Ospedaliero Cantonale,
6500 Bellinzona, Switzerland
6
Faculty of Biology and Medicine, University of Lausanne, 1015 Lausanne, Switzerland
7
Faculty of Biomedical Sciences, Università della Svizzera italiana, 6900 Lugano, Switzerland
* Correspondence: giorgio.treglia@eoc.ch (G.T.); francesco.giovinazzo@policlinicogemelli.it (F.G.)
Simple Summary: Robust predictive and prognostic tools are needed in the management of breast
cancer liver metastases (BCLMs). Until now, surgery has not been the gold standard of treatment
of patients with BCLMs. The present manuscript highlights several predictive factors related to
the primary tumor and the BCLM that may help to identify candidates for surgery with favorable
outcomes in a large cohort of patients.
Abstract: Background: The role of surgical resection of liver metastases in patients with breast cancer
liver metastasis (BCLM) remains controversial. A systematic review and meta-analysis of prognostic
factors related to survival after BCLM resection was performed. Methods: An electronic search of
relevant publications was performed. Pooled outcome measures were expressed as hazard ratios
(HRs), including 95% confidence interval values (95% CIs), and calculated through a random-effects
model. Heterogeneity was tested through the I
2
index. Results: Thirty-five publications reported
analyses on prognostic factors and survival. A total of 2782 patients who underwent liver resection for
BCLM were included. Positive axillary lymph nodes at breast cancer diagnosis were an unfavorable
survival factor (HR 1.74, 95% CI 1.25 to 2.41, I
2
= 0%). Cumulative predictive factor HRs (multiple
liver metastases, size of the metastases, short interval between primary tumor and onset of liver
disease) related to the BCLM pattern were 1.32 (95% CI 1.17 to 1.48, I
2
= 71%) and 1.51 (95% CI
1.15 to 1.98, I
2
= 76%) for surgical and pathological features (resection margin and presence of
extrahepatic disease), respectively. Conclusion: Resection of BCLM may provide a survival benefit
for selected patients. For better long-term results, surgical selection should consider both primary
tumor and BCLM features such as negative axillary lymph nodes at breast resection, a single hepatic
lesion, a time longer than 24 months between breast and hepatic diagnosis, and a realizable R0 liver
resection. However, the high heterogeneity among studies suggests the need for an RCT to validate
the present findings.
Keywords: breast cancer; liver metastases; hepatic resection; prognostic factors; meta-analysis
Cancers 2022, 14, 1691. https://doi.org/10.3390/cancers14071691 https://www.mdpi.com/journal/cancers