Influence of the Type and Rate of Subarachnoid Fluid Infusion on Lethal Neurogenic Pulmonary Edema in Rats

Abstract

In patients who experience sudden death from spontaneous subarachnoid hemorrhage, more than 90% present with acute pulmonary edema. The underlying pathogenesis of this complication is poorly understood. In addition, the specific role of the extravasated blood products and the associated elevation in intracranial pressure leading to the systemic and pulmonary effects during subarachnoid hemorrhage are not well established. The authors tested a new model of acute and severe subarachnoid hemorrhage comparing fresh whole autologous blood (n = 20) with 5% albumin (n = 19) injected at two different rates (35 seconds versus 24 minutes) into the cisterna magna of anesthetized, mechanically ventilated rats. Cerebral and systemic hemodynamics and the corresponding pulmonary function were evaluated. The type of fluid injected had no influence on survival or hemodynamic and respiratory parameters. Rapid infusion of either blood or albumin (n = 14) produced an acute and transient rise in intracranial pressure (37.9 +/- 3.5 mm Hg) associated with systemic hypertension and increased cerebral perfusion pressure that was sustained in survivors but not in nonsurvivors. Slow infusion (n = 23) produced a more progressive increase in intracranial pressure to 31.2 +/- 7.1 mm Hg with a parallel and sustained increase of systemic blood pressure and preserved cerebral perfusion pressure in survivors, but produced a pattern of more severe hypertension followed by hypotension in nonsurvivors. Sixty-four percent of animals (rapid infusion) and 48% of animals (slow infusion) survived the challenge and presented no pulmonary alterations. In contrast, nonsurviving rats developed reduced lung compliance and gas exchange, an increased alveolar-arterial protein concentration ratio (0.36 +/- 0.02 versus 0.17 +/- 0.03 in survivors; P <.0001), and increased lung weight (5.7 +/- 0.3 g versus 2.0 +/- 0.1 g; P <.0001), demonstrating a fulminant increased permeability pulmonary edema, leading to death within one hour. These results indicate that the chosen rapid- and slow-injection rates resulted in a similar death rate of 50%. Mortality was similar for blood and albumin administration, pulmonary edema occurred in nonsurvivors in both the rapid- and slow-injection groups, and pulmonary edema is associated with more severe hypertension in the slow-injection group. Furthermore, these results suggest that the development of neurogenic pulmonary edema that is characterized by an acutely increased capillary permeability to proteins is independent of the degree of intracranial pressure increase or the type of fluid administrated.

Time and tidal volume-dependent ventilator-induced lung injury in healthy rats

“…The alveolar-arterial protein concentration ratio used in this model has some limitations. This ratio is an estimate of pulmonary permeability [19,20]; however, protein measurement in BAL may also include proteins from the local inflammatory reaction and surfactant proteins. Thus, the reported alveolar-arterial protein concentration ratio may be an overestimation of the pulmonary permeability.…”

“…Total protein concentration (plasma and BAL fluid proteins) at the end of the experiment (or just before death, if applicable) was measured in the supernatant by spectrophotometry (Bio-Rad Protein Assay; Bio-Rad Laboratories, Hercules, CA). The alveolar-arterial protein concentration ratio between alveolar and arterial plasma protein concentration per group was calculated to estimate pulmonary permeability [19,20].…”

Early Events After Aneurysmal Subarachnoid Hemorrhage

“…Pulmonary edema usually develops within after SAH, mechanisms that the CR activates, and the complications that follow; and ( c ) outlines the main mechanism by which transient global ischemia contributes to early brain injury after SAH hours after SAH; however, a delayed form that appears 3-5 days after SAH is also reported [ 35 ]. In animals, leakage of lung capillaries occurs 8 min after injection of blood into the cisterna magna [ 36 ]. The nature of mechanisms underlying SAH-related pulmonary edema are cardiogenic (myocardial dysfunction leading to a raised hydrostatic pressure and fl uid retention), noncardiogenic (such as acute lung injury or acute respiratory distress syndrome), and neurogenic (pressure of blood on respiratory centers at SAH) [ 34 , 35 ].…”

Neurogenic pulmonary edema caused by spontaneous cerebellar hemorrhage: A fatal case report

“…[19] Moreover, it was reported that the amount, but not the type of fluid injected intrathecally had a significant impact on hemodynamic and respiratory parameters. [22]…”