Blood Flow and Shear Stress Allow Monitoring of Progression and Prognosis of Tumor Diseases

Matthias Barral; Imane El-Sanharawi; Anthony Dohan; Maxime Sebuhyan; Alexis Guedon; Audrey Delarue; Alexandre Boutigny; Nassim Mohamedi; Benjamin Magnan; Salim Kemel; Chahinez Ketfi; Nathalie Kubis; Annouk Bisdorff-Bresson; Marc Pocard; Philippe Bonnin

doi:10.3389/fphys.2021.693052

Blood Flow and Shear Stress Allow Monitoring of Progression and Prognosis of Tumor Diseases

Front Physiol. 2021 Aug 3:12:693052. doi: 10.3389/fphys.2021.693052. eCollection 2021.

Authors

Matthias Barral¹, Imane El-Sanharawi², Anthony Dohan¹, Maxime Sebuhyan², Alexis Guedon², Audrey Delarue², Alexandre Boutigny^{2

3}, Nassim Mohamedi², Benjamin Magnan², Salim Kemel², Chahinez Ketfi², Nathalie Kubis^{2

3}, Annouk Bisdorff-Bresson⁴, Marc Pocard^{1

5}, Philippe Bonnin^{2

3}

Affiliations

¹ INSERM UMR1275, Université de Paris, Hôpital Lariboisière, Paris, France.
² AP-HP, Université de Paris, Hôpital Lariboisière, Physiologie Clinique - Explorations Fonctionnelles, Paris, France.
³ INSERM UMR1148 - LVTS, Université de Paris, Hôpital Bichat, Paris, France.
⁴ AP-HP, Université de Paris, Hôpital Lariboisière, Neuroradiologie, Centre Constitutif des Malformations Artério Veineuses Superficielles de l'Enfant et de l'Adulte, Paris, France.
⁵ AP-HP, Sorbonne-Université, Hôpital Pitié-Salpêtrière, Chirurgie Digestive et Cancérologique, Paris, France.

Abstract

In the presence of tumor angiogenesis, blood flow must increase, leading to an elevation of blood flow velocities (BFVels) and wall shear stress (WSS) in upstream native arteries. An adaptive arterial remodeling is stimulated, whose purpose lies in the enlargement of the arterial inner diameter, aiming for normalization of BFVels and WSS. Remodeling engages delayed processes that are efficient only several weeks/months after initiation, independent from those governing expansion of the neovascular network. Therefore, during tumor expansion, there is a time interval during which elevation of BFVels and WSS could reflect disease progression. Conversely, during the period of stability, BFVels and WSS drop back to normal values due to the achievement of remodeling processes. Ovarian peritoneal carcinomatosis (OPC), pseudomyxoma peritonei (PMP), and superficial arteriovenous malformations (AVMs) are diseases characterized by the development of abnormal vascular networks developed on native ones. In OPC and PMP, preoperative blood flow in the superior mesenteric artery (SMA) correlated with the per-operative peritoneal carcinomatosis index (OPC: n = 21, R = 0.79, p < 0.0001, PMP: n = 66, R = 0.63, p < 0.0001). Moreover, 1 year after surgery, WSS in the SMA helped in distinguishing patients with PMP from those without disease progression [ROC-curve analysis, AUC = 0.978 (0.902-0.999), p < 0.0001, sensitivity: 100.0%, specificity: 93.5%, cutoff: 12.1 dynes/cm²]. Similarly, WSS in the ipsilateral afferent arteries close to the lesion distinguished stable from progressive AVM [ROC-curve analysis, AUC: 0.988, (0.919-1.000), p < 0.0001, sensitivity: 93.5%, specificity: 95.7%; cutoff: 26.5 dynes/cm²]. Blood flow volume is indicative of the tumor burden in OPC and PMP, and WSS represents an early sensitive and specific vascular marker of disease progression in PMP and AVM.

Keywords: arteriovenous malformation; blood flow velocity; carotid artery; disease progression; peritoneal carcinomatosis; pseudomyxoma peritonei; superior mesenteric artery; wall shear stress.