Hirudin ameliorates intestinal radiation toxicity in the rat: support for thrombin inhibition as strategy to minimize side-effects after radiation therapy and as countermeasure against radiation exposure

J Thromb Haemost. 2004 Nov;2(11):2027-35. doi: 10.1111/j.1538-7836.2004.00960.x.

Abstract

Background: The small bowel is a dose-limiting normal tissue in radiation therapy of malignancies in the abdomen and pelvis, as well as an important determinant of survival after non-therapeutic radiation exposure. Irradiation of normal tissues, including intestine, causes loss of vascular thromboresistance and upregulation of thrombin receptors. Radiation-induced endothelial dysfunction is thought to be involved in both early and delayed radiation responses. Hence, thrombin may be a potential target for ameliorating normal tissue radiation toxicity.

Objective: To assess direct thrombin inhibition as a protective strategy against small bowel radiation toxicity.

Methods: Rat small intestine was exposed to localized orthovoltage X-radiation. Recombinant hirudin, a direct thrombin inhibitor, or vehicle was infused from 2 days before irradiation to 14 days after irradiation. Structural, cellular, and molecular aspects of intestinal radiation injury were assessed at 2 weeks (early toxicity) and 26 weeks (chronic toxicity) after irradiation.

Results: Compared with unirradiated intestine, irradiated intestine showed increased expression of tissue factor, increased immunoreactivity for enzymatically active thrombin, and increased extravascular fibrin(ogen) deposition. Hirudin treatment significantly attenuated radiation-induced mucosal damage (P = 0.04), reactive intestinal wall thickening (P = 0.02), transforming growth factor-beta immunoreactivity levels (P = 0.0002), and collagen III deposition (P = 0.003). The differences between hirudin-treated and control rats were more pronounced at 2 weeks than at 26 weeks after irradiation. Hirudin treatment did not affect postradiation granulocyte infiltration.

Conclusions: Short-term thrombin inhibition attenuates important aspects of intestinal radiation toxicity. Thrombin is a promising target for minimizing normal tissue injury after radiation therapy of cancer, as well as for protecting normal tissues from the adverse effects of non-therapeutic radiation exposure.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Animals
  • Fibrin / analysis
  • Fibrin / genetics
  • Gamma Rays / adverse effects*
  • Hirudins / pharmacology*
  • Intestinal Diseases / drug therapy*
  • Intestinal Diseases / etiology
  • Intestinal Diseases / pathology
  • Intestines / chemistry
  • Intestines / pathology
  • Intestines / radiation effects*
  • Male
  • RNA, Messenger / analysis
  • Radiation Injuries / drug therapy
  • Radiation Tolerance / drug effects*
  • Radiation-Protective Agents / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Thrombin / analysis
  • Thrombin / antagonists & inhibitors
  • Thrombin / genetics
  • Thromboplastin / analysis
  • Thromboplastin / genetics

Substances

  • Hirudins
  • RNA, Messenger
  • Radiation-Protective Agents
  • Fibrin
  • Thromboplastin
  • Thrombin