Physiological Conditions Associated with Stress Failure of Pulmonary Capillaries

The most remarkable physiological situation where stress failure of pulmonary capillaries is seen is in galloping thoroughbred racehorses. There is now evidence that all thoroughbreds in training bleed into their lungs. This condition, called exercise-induced pulmonary hemorrhage, has been known since Elizabethan times, and all sorts of explanations have been offered such as moldy hay. However, recently it has become apparent that exercising thoroughbreds have extremely high pulmonary vascular pressures. For example, studies on animals galloping on a treadmill show that a left atrial pressure measured directly with a catheter can be as high as 70 mmHg, and this is associated with a mean pulmonary artery pressure as high as 120mmHg. Other vascular pressures are equally astonishing, with a mean systemic arterial pressure as high as 240 mmHg and a mean right atrial pressure up to 40 mmHg.

The reason for these high pressures is that these animals have been selectively bred for hundreds of years for very high aerobic performances. As examples, their maximal oxygen consumptions reach 180mLmin-1kg-1 and cardiac outputs are as high as 750 mLmin-1kg-1. In order to develop these extraordinary cardiac outputs the filling pressures of the left ventricle must be very high, and this in turn translates to high pulmonary venous and capillary pressures. We have looked at the lungs of thoroughbreds immediately after they have been galloped on a treadmill and shown unequivocal evidence of breaks in the pulmonary capillaries [9].

These extraordinary findings in racehorses raise the question of whether elite human athletes ever develop ultrastructural changes in their pulmonary capillaries during maximal exercise. There is now strong evidence for this. Six elite cyclists sprinted uphill over several minutes at maximal effort sufficient to give a mean heart rate of 177 beats minute-1, and within an hour they voluntarily underwent bronchoalveolar lavage (BAL). The results were compared with those of normal sedentary subjects who did not exercise before BAL, and it was found that the athletes had significantly higher concentrations of red blood cells, total protein, albumin, and leukotriene B4 (LTB4) in their BAL fluid compared with the control subjects [10]. Thus brief but very intense exercise in elite athletes apparently causes changes in the integrity of the capillary wall.

Would the same changes occur if the athletes worked for a longer period at slightly lower levels of exercise? This was tested by making additional measurements on a similar group of six elite cyclists who exercised at 77 percent of their maximal work level for 1 hour and then underwent BAL. Again the controls were eight normal nonathletes who did not exercise before BAL. In contrast to the results of the previous studies, these athletes showed no differences compared with the controls. Thus we can conclude that only extremely high levels of exercise cause changes in the capillary walls, and indeed this is what might be expected

Table I Pathological Conditions Causing Stress Failure of the Blood-Gas Barrier.

1. High capillary pressure resulting in high-permeability edema, e.g., high-altitude pulmonary edema, neurogenic pulmonary edema

2. High capillary pressure causing edema and hemorrhage, e.g., mitral stenosis, left ventricular failure

3. High state of lung inflation, e.g., positive end-expiratory pressure in the intensive care unit

4. Abnormal extracellular matrix, e.g., Goodpasture's syndrome on evolutionary lines. In general organisms evolve to cope with all but the most extreme stresses to which they are subjected.

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