DCE-MRI and Quantitative Histology Reveal Enhanced Vessel Maturation but Impaired Perfusion and Increased Hypoxia in Bevacizumab-Treated Cervical Carcinoma

Int J Radiat Oncol Biol Phys. 2019 Jul 1;104(3):666-676. doi: 10.1016/j.ijrobp.2019.03.002. Epub 2019 Mar 8.

Abstract

Purpose: This study had a dual purpose: to investigate (1) whether bevacizumab can change the microvasculature and oxygenation of cervical carcinomas and (2) whether any changes can be detected with dynamic contrast-enhanced magnetic resonance imaging (DCE-MRI).

Methods and materials: Two patient-derived xenograft models of cervical cancer (BK-12 and HL-16) were included in the study. Immunostained histologic preparations from untreated and bevacizumab-treated tumors were analyzed with respect to microvascular density, vessel pericyte coverage, and tumor hypoxia using CD31, α-SMA, and pimonidazole as markers, respectively. DCE-MRI was performed at 7.05 T, and parametric images of Ktrans and ve were derived from the data using the Tofts pharmacokinetic model.

Results: The tumors of both models showed decreased microvascular density, increased vessel pericyte coverage, and increased vessel maturation after bevacizumab treatment. Bevacizumab-treated tumors were more hypoxic and had lower Ktrans values than untreated tumors in the BK-12 model, whereas bevacizumab-treated and untreated HL-16 tumors had similar hypoxic fractions and similar Ktrans values. Significant correlations were found between median Ktrans and hypoxic fraction, and the data for untreated and bevacizumab-treated tumors were well fitted by the same curve in both tumor models.

Conclusions: Bevacizumab-treated tumors show less abnormal microvessels than untreated tumors do, but because of treatment-induced vessel pruning, the overall function of the microvasculature might be impaired after bevacizumab treatment, resulting in increased tumor hypoxia. DCE-MRI has great potential for monitoring bevacizumab-induced changes in tumor hypoxia in cervical carcinoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins
  • Angiogenesis Inhibitors / pharmacology*
  • Animals
  • Bevacizumab / pharmacology*
  • Capillary Permeability / drug effects
  • Contrast Media
  • Female
  • Heterografts
  • Humans
  • Magnetic Resonance Imaging / methods
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Microvessels / drug effects*
  • Microvessels / pathology
  • Nitroimidazoles
  • Oxygen Consumption / drug effects
  • Pericytes / drug effects
  • Tumor Hypoxia / drug effects*
  • Tumor Microenvironment / drug effects
  • Uterine Cervical Neoplasms / blood supply*
  • Uterine Cervical Neoplasms / metabolism*

Substances

  • ACTA2 protein, human
  • Actins
  • Angiogenesis Inhibitors
  • Contrast Media
  • Nitroimidazoles
  • Bevacizumab
  • pimonidazole