Contemporaneous Perioperative Inflammatory and Angiogenic Cytokine Profiles of Surgical Breast, Colorectal, and Prostate Cancer Patients: Clinical Implications

Surgery-induced tumor growth acceleration and synchronous metastatic growth promotion have been observed for decades. Surgery-induced wound healing, orchestrated through growth factors, chemokines, and cytokines, can negatively impact patients harboring residual or metastatic disease. We provide det...

Full description

Bibliographic Details
Main Authors: Leili Baghaie, Fiona Haxho, Fleur Leroy, Beth Lewis, Alexander Wawer, Shamano Minhas, William W. Harless, Myron R. Szewczuk
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/12/23/2767
_version_ 1797400295402110976
author Leili Baghaie
Fiona Haxho
Fleur Leroy
Beth Lewis
Alexander Wawer
Shamano Minhas
William W. Harless
Myron R. Szewczuk
author_facet Leili Baghaie
Fiona Haxho
Fleur Leroy
Beth Lewis
Alexander Wawer
Shamano Minhas
William W. Harless
Myron R. Szewczuk
author_sort Leili Baghaie
collection DOAJ
description Surgery-induced tumor growth acceleration and synchronous metastatic growth promotion have been observed for decades. Surgery-induced wound healing, orchestrated through growth factors, chemokines, and cytokines, can negatively impact patients harboring residual or metastatic disease. We provide detailed clinical evidence of this process in surgical breast, prostate, and colorectal cancer patients. Plasma samples were analyzed from 68 cancer patients who had not received treatment before surgery or adjuvant therapy until at least four weeks post-surgery. The levels of plasma cytokines, chemokines, and growth factors were simultaneously quantified and profiled using multiplexed immunoassays for eight time points sampled per patient. The immunologic processes are induced immediately after surgery in patients, characterized by a drastic short-term shift in the expression levels of pro-inflammatory and angiogenic molecules and cytokines. A rapid and significant spike in circulating plasma levels of hepatocyte growth factor (HGF), interleukin-6 (IL-6), placental growth factor (PLGF), and matrix metalloproteinase-9 (MMP-9) after surgery was noted. The rise in these molecules was concomitant with a significant drop in transforming growth factor-β1 (TGF-β1), platelet-derived growth factor (PDGF-AB/BB), insulin-like growth factor-1 (IGF-1), and monocyte chemoattractant protein-2 (MCP-2). If not earlier, each plasma analyte was normalized to baseline levels within 1–2 weeks after surgery, suggesting that surgical intervention alone was responsible for these effects. The effects of surgical tumor removal on disrupting the pro-inflammatory and angiogenic plasma profiles of cancer patients provide evidence for potentiating malignant progression. Our findings indicate a narrow therapeutic window of opportunity after surgery to prevent disease recurrence.
first_indexed 2024-03-09T01:53:29Z
format Article
id doaj.art-150cfeac151344a49ec2a3c4501e7cca
institution Directory Open Access Journal
issn 2073-4409
language English
last_indexed 2024-03-09T01:53:29Z
publishDate 2023-12-01
publisher MDPI AG
record_format Article
series Cells
spelling doaj.art-150cfeac151344a49ec2a3c4501e7cca2023-12-08T15:13:17ZengMDPI AGCells2073-44092023-12-011223276710.3390/cells12232767Contemporaneous Perioperative Inflammatory and Angiogenic Cytokine Profiles of Surgical Breast, Colorectal, and Prostate Cancer Patients: Clinical ImplicationsLeili Baghaie0Fiona Haxho1Fleur Leroy2Beth Lewis3Alexander Wawer4Shamano Minhas5William W. Harless6Myron R. Szewczuk7Department of Biomedical & Molecular Sciences, Queen’s University, Kingston, ON K7L 3N6, CanadaDepartment of Biomedical & Molecular Sciences, Queen’s University, Kingston, ON K7L 3N6, CanadaDepartment of Biomedical & Molecular Sciences, Queen’s University, Kingston, ON K7L 3N6, CanadaENCYT Technologies Inc., Membertou, NS B1S 0H1, CanadaENCYT Technologies Inc., Membertou, NS B1S 0H1, CanadaENCYT Technologies Inc., Membertou, NS B1S 0H1, CanadaENCYT Technologies Inc., Membertou, NS B1S 0H1, CanadaDepartment of Biomedical & Molecular Sciences, Queen’s University, Kingston, ON K7L 3N6, CanadaSurgery-induced tumor growth acceleration and synchronous metastatic growth promotion have been observed for decades. Surgery-induced wound healing, orchestrated through growth factors, chemokines, and cytokines, can negatively impact patients harboring residual or metastatic disease. We provide detailed clinical evidence of this process in surgical breast, prostate, and colorectal cancer patients. Plasma samples were analyzed from 68 cancer patients who had not received treatment before surgery or adjuvant therapy until at least four weeks post-surgery. The levels of plasma cytokines, chemokines, and growth factors were simultaneously quantified and profiled using multiplexed immunoassays for eight time points sampled per patient. The immunologic processes are induced immediately after surgery in patients, characterized by a drastic short-term shift in the expression levels of pro-inflammatory and angiogenic molecules and cytokines. A rapid and significant spike in circulating plasma levels of hepatocyte growth factor (HGF), interleukin-6 (IL-6), placental growth factor (PLGF), and matrix metalloproteinase-9 (MMP-9) after surgery was noted. The rise in these molecules was concomitant with a significant drop in transforming growth factor-β1 (TGF-β1), platelet-derived growth factor (PDGF-AB/BB), insulin-like growth factor-1 (IGF-1), and monocyte chemoattractant protein-2 (MCP-2). If not earlier, each plasma analyte was normalized to baseline levels within 1–2 weeks after surgery, suggesting that surgical intervention alone was responsible for these effects. The effects of surgical tumor removal on disrupting the pro-inflammatory and angiogenic plasma profiles of cancer patients provide evidence for potentiating malignant progression. Our findings indicate a narrow therapeutic window of opportunity after surgery to prevent disease recurrence.https://www.mdpi.com/2073-4409/12/23/2767surgery-induced wound healinggrowth factorschemokinescytokinessurgical breastprostate
spellingShingle Leili Baghaie
Fiona Haxho
Fleur Leroy
Beth Lewis
Alexander Wawer
Shamano Minhas
William W. Harless
Myron R. Szewczuk
Contemporaneous Perioperative Inflammatory and Angiogenic Cytokine Profiles of Surgical Breast, Colorectal, and Prostate Cancer Patients: Clinical Implications
Cells
surgery-induced wound healing
growth factors
chemokines
cytokines
surgical breast
prostate
title Contemporaneous Perioperative Inflammatory and Angiogenic Cytokine Profiles of Surgical Breast, Colorectal, and Prostate Cancer Patients: Clinical Implications
title_full Contemporaneous Perioperative Inflammatory and Angiogenic Cytokine Profiles of Surgical Breast, Colorectal, and Prostate Cancer Patients: Clinical Implications
title_fullStr Contemporaneous Perioperative Inflammatory and Angiogenic Cytokine Profiles of Surgical Breast, Colorectal, and Prostate Cancer Patients: Clinical Implications
title_full_unstemmed Contemporaneous Perioperative Inflammatory and Angiogenic Cytokine Profiles of Surgical Breast, Colorectal, and Prostate Cancer Patients: Clinical Implications
title_short Contemporaneous Perioperative Inflammatory and Angiogenic Cytokine Profiles of Surgical Breast, Colorectal, and Prostate Cancer Patients: Clinical Implications
title_sort contemporaneous perioperative inflammatory and angiogenic cytokine profiles of surgical breast colorectal and prostate cancer patients clinical implications
topic surgery-induced wound healing
growth factors
chemokines
cytokines
surgical breast
prostate
url https://www.mdpi.com/2073-4409/12/23/2767
work_keys_str_mv AT leilibaghaie contemporaneousperioperativeinflammatoryandangiogeniccytokineprofilesofsurgicalbreastcolorectalandprostatecancerpatientsclinicalimplications
AT fionahaxho contemporaneousperioperativeinflammatoryandangiogeniccytokineprofilesofsurgicalbreastcolorectalandprostatecancerpatientsclinicalimplications
AT fleurleroy contemporaneousperioperativeinflammatoryandangiogeniccytokineprofilesofsurgicalbreastcolorectalandprostatecancerpatientsclinicalimplications
AT bethlewis contemporaneousperioperativeinflammatoryandangiogeniccytokineprofilesofsurgicalbreastcolorectalandprostatecancerpatientsclinicalimplications
AT alexanderwawer contemporaneousperioperativeinflammatoryandangiogeniccytokineprofilesofsurgicalbreastcolorectalandprostatecancerpatientsclinicalimplications
AT shamanominhas contemporaneousperioperativeinflammatoryandangiogeniccytokineprofilesofsurgicalbreastcolorectalandprostatecancerpatientsclinicalimplications
AT williamwharless contemporaneousperioperativeinflammatoryandangiogeniccytokineprofilesofsurgicalbreastcolorectalandprostatecancerpatientsclinicalimplications
AT myronrszewczuk contemporaneousperioperativeinflammatoryandangiogeniccytokineprofilesofsurgicalbreastcolorectalandprostatecancerpatientsclinicalimplications