Antithrombin attenuates vascular leakage via inhibiting neutrophil activation in acute lung injury

Crit Care Med. 2013 Dec;41(12):e439-46. doi: 10.1097/CCM.0b013e318298ad3a.

Abstract

Objective: To test the hypothesis that restoration of antithrombin plasma concentrations attenuates vascular leakage by inhibiting neutrophil activation through syndecan-4 receptor inhibition in an established ovine model of acute lung injury.

Design: Randomized controlled laboratory experiment.

Setting: University animal research facility.

Subjects: Eighteen chronically instrumented sheep.

Interventions: Following combined burn and smoke inhalation injury (40% of total body surface area, third-degree flame burn; 4 × 12 breaths of cold cotton smoke), chronically instrumented sheep were randomly assigned to receive an IV infusion of 6 IU/kg/hr recombinant human antithrombin III or normal saline (n = 6 each) during the 48-hour study period. In addition, six sham animals (not injured, continuous infusion of vehicle) were used to obtain reference values for histological and immunohistochemical analyses.

Measurements and main results: Compared to control animals, recombinant human antithrombin III reduced the number of neutrophils per hour in the pulmonary lymph (p < 0.01 at 24 and 48 hr), alveolar neutrophil infiltration (p = 0.04), and pulmonary myeloperoxidase activity (p = 0.026). Flow cytometric analysis revealed a significant reduction of syndecan-4-positive neutrophils (p = 0.002 vs control at 24 hr). Treatment with recombinant human antithrombin III resulted in a reduction of pulmonary nitrosative stress (p = 0.002), airway obstruction (bronchi: p = 0.001, bronchioli: p = 0.013), parenchymal edema (p = 0.044), and lung bloodless wet-to-dry-weight ratio (p = 0.015). Clinically, recombinant human antithrombin III attenuated the increased pulmonary transvascular fluid flux (12-48 hr: p ≤ 0.001 vs control each) and the deteriorated pulmonary gas exchange (12-48 hr: p < 0.05 vs control each) without increasing the risk of bleeding.

Conclusions: The present study provides evidence for the interaction between antithrombin and neutrophils in vivo, its pathophysiological role in vascular leakage, and the therapeutic potential of recombinant human antithrombin III in a large animal model of acute lung injury.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acute Lung Injury / drug therapy*
  • Acute Lung Injury / etiology
  • Acute Lung Injury / pathology
  • Acute Lung Injury / physiopathology*
  • Airway Obstruction / drug therapy
  • Animals
  • Antithrombin III / therapeutic use*
  • Antithrombins / therapeutic use*
  • Burns / complications
  • Capillary Permeability / drug effects*
  • Cell Movement / drug effects
  • Disease Models, Animal
  • Edema / drug therapy
  • Female
  • Lung / enzymology
  • Lung / pathology
  • Neutrophil Activation / drug effects*
  • Neutrophils / metabolism
  • Neutrophils / physiology*
  • Peroxidase / metabolism
  • Pulmonary Gas Exchange / drug effects
  • Random Allocation
  • Receptors, G-Protein-Coupled / metabolism*
  • Recombinant Proteins / therapeutic use
  • Sheep
  • Smoke Inhalation Injury / complications
  • Syndecan-4 / metabolism

Substances

  • Antithrombins
  • Receptors, G-Protein-Coupled
  • Recombinant Proteins
  • Syndecan-4
  • Antithrombin III
  • Peroxidase