Pulmonary edema following fatal aneurysm rupture

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✓ A retrospective clinico-pathological analysis of 78 cases of fatal subarachnoid hemorrhage (SAH) was carried out: 71% had a pathological diagnosis of pulmonary edema (PE), and of these 31% had a clinical diagnosis of PE. Patients with pathological PE were younger and died sooner after their SAH than those without. The incidence of PE fell with the passage of time following SAH, while the occurrence of pneumonia and embolism increased. There were hypoxemia and hypocapnia in both groups, more severe in the group that had pathological PE. The pathophysiology of neurogenic PE is discussed and possible therapeutic approaches indicated.

Abstract

✓ A retrospective clinico-pathological analysis of 78 cases of fatal subarachnoid hemorrhage (SAH) was carried out: 71% had a pathological diagnosis of pulmonary edema (PE), and of these 31% had a clinical diagnosis of PE. Patients with pathological PE were younger and died sooner after their SAH than those without. The incidence of PE fell with the passage of time following SAH, while the occurrence of pneumonia and embolism increased. There were hypoxemia and hypocapnia in both groups, more severe in the group that had pathological PE. The pathophysiology of neurogenic PE is discussed and possible therapeutic approaches indicated.

Pulmonary edema (PE) has been recorded in isolated case reports following subarachnoid hemorrhage (SAH) from aneurysm rupture.4,7 Weisman23 reported a significant increase compared to controls in the combined lung weight of patients who died from intracranial hemorrhage. He concluded that PE and congestion develop to a severe degree almost immediately after intracranial hemorrhage. Crompton,5 in an autopsy series of ruptured aneurysms, found that one-third of the cases had PE, despite the fact that those who died within the first day of admission were excluded from his series. The present study is a retrospective analysis of the clinical and pathological data on 78 cases of fatal SAH from ruptured aneurysm. Pulmonary edema is defined as an increased water content in the lung, interstitial and/or alveolar, and was diagnosed pathologically by the gross findings of increased lung weight and the presence of serosanguinous fluid in the airways, which also oozed from the cut surface of the lung.

Observations
Pathological Pulmonary Edema Group

Between 1967 and 1977, 141 patients died from ruptured aneurysms. Of these, 83 (59%) were autopsied. Five cases had autopsy limited to the head. A diagnosis of PE was made at autopsy by the pathologist in 55 (71%) of these cases.

The patients with pathological PE tended to be younger, died more quickly, and consequently had fewer operations than those without (Table 1), but this difference was not statistically significant (p > 0.05). All the patients with pathological PE had fresh SAH at the time of autopsy, whereas in some of those without PE sufficient time had elasped since the onset of their illness for the gross evidence of this to have disappeared. There was no difference with respect to the types of associated intracranial hemorrhage or associated systemic disease. There was a significantly higher incidence of cerebral edema (CE) in the group with pathological PE than in the group without. There were also more middle cerebral aneurysms in this group but the difference was not statistically significant (Table 2).

TABLE 1

Comparison of clinical data between groups with and without pathological diagnosis of pulmonary edema (PE) at autopsy

Clinical DataCases With Pathological PECases Without Pathological PE
no. of cases5523
age (yrs)47 ± 14*52 ± 17*
patients dying 1st
 day (%)3219
patients operated
 on (%)4554
survival SAH to
 death (days)10 ± 15*21 ± 44*
patients with only
 one SAH (%)8596

Values are shown as mean ± standard deviation. Differences are not significant (p > 0.05)

TABLE 2

Comparison of pathological findings in patients with and without pathological diagnosis of pulmonary edema (PE) at autopsy

Pathological DataCases With Pathological PE (%)Cases Without Pathological PE (%)
subarachnoid
 hemorrhage10088
intracerebral
 hemorrhage4150
intraventricular
 hemorrhage2629
midbrain
 hemorrhage1213
subdural
 hemorrhage1216
extradural
 hemorrhage24
site of aneurysm
 middle cerebral4633
 anterior cerebral2537
 internal carotid1715
 vertebral basilar1215
 multiple127
cerebral edema92*71*
systemic
 atherosclerosis4946
renal disease1929

Significant difference (p < 0.05) by chi-square and Z-test of sample proportions. Other differences were not significant.

The duration of survival following SAH had an important bearing on the frequency of pulmonary pathological findings. In patients who died shortly after SAH, PE and congestion were very common but diminished in frequency as post-SAH survival increased, as did the frequency of pulmonary effusions. In contrast, the incidence of pneumonia and embolism steadily increased. The finding of CE and hippocampal and/or tonsillar herniation decreased with time after SAH, but the opposite was true for cerebral infarction (Table 3).

TABLE 3

Pathological findings in the lung and brain by time interval between last subarachnoid hemorrhage (SAH) and death

Pathological FindingsSurvival Post-SAH (days)
1–34–14> 14 
lung (%)
 pulmonary edema90*62*52*
 pulmonary congestion967474
 pneumonia193550
 effusions1154
 adhesions11430
 emphysema101014
 embolismO1220
brain (%)
 cerebral edema967474
 cerebral infarction19*48*70*
 hippocampal and/or
  tonsillar herniation787452

Significant differences by chi-square test of association, p < 0.01.

Significant differences by chi-square test of association, p < 0.05.

The initial blood-gas determinations before the institution of oxygen therapy demonstrated a marked reduction in PaO2 and PaCO2. The deviation from normal was greater in the group that subsequently died with pathological PE. In both groups, PaO2 was brought to higher levels with oxygen therapy (Table 4).

TABLE 4

Arterial blood-gas findings in groups with and without the pathological diagnosis of pulmonary edema (PE) at autopsy

Blood-Gas DataPathological PENo Pathological PE
InitialAfter Oxygen Therapy*Initial After Oxygen Therapy 
PaO2 (mm Hg)48 ± 12† 160 ± 92 62 ± 9†152 ± 98 
PaCO2 (mm Hg)27 ± 9 27 ± 7 32 ± 531 ± 4 
pH7.41 ± 0.12 7.49 ± 0.09 7.47 ± 0.057.46 ± 0.08 
O2 saturation (%)85 ± 14 98 ± 3 92 ± 597 ± 8 

When multiple determinations were made, the set of values with the highest PaO2 was used in this comparison.

Significant difference (p < 0.05) by t-test for comparison of two sample means. Other differences were not significant.

Clinical Pulmonary Edema Group

Eighteen patients were believed to have shown good evidence of clinical PE on retrospective analysis. All but one of them also had a pathological diagnosis of PE, and in that case autopsy was limited to the head only. The following contemporary clinical impression was recorded in 93% of these cases: sudden onset of coma was universal; in the cases in which the ictus was witnessed (18%), the breathing difficulties started within minutes; 94% were deeply comatose at the time of the diagnosis of clinical PE, only one was described as being arousable; 33% had a history of vomiting; a pink foam was observed in the airways of all with the clinical diagnosis of PE; 82% were cyanotic and respirations were described as Cheyne-Stokes in 87%; 91% had radiological evidence of PE; when observations on the skin were made, it was described as moist and cool.

The clinical PE group had a mean age of 58 ± 44 years, but the mean was influenced by the occurrence of three cases over the age of 70. Of this group, 83% were under the age of 50 years, making it a more youthful group than patients with ruptured aneurysms as a whole. In 66%, death occurred the first day, and the mean survival was 1.6 ± 0.9 days. Four cases were operated on, but in three cases the operation preceded the final fatal SAH which induced the PE. These operations were a proximal clipping, carotid ligation, and aneurysm wrapping. The fourth patient underwent bitemporal decompression following the final SAH.

Mean admission values were: systolic blood pressure (BP), 164 ± 50 mm Hg: diastolic BP, 92 ± 28 mm Hg; temperature 37.4° ± 0.9°; heart rate, 88 ± 31; respiratory rate, 23 ± 8. In the clinical PE group, 72% had a systolic BP of > 150, and 61% had diastolic BP of > 100; 44% had a heart rat > 100, and 19% had a heart rate ≤ 60. Nine patients had electrocardiograms performed 44% showed sinus tachycardia, 33% ventricular fibrillation, 33% inverted T waves, 11% S-T depression, and 11% heart block with nodal rhythm. Respiratory rate was ≥ 30 in 18% of these patients, and 12% were apneic on arrival at the emergency room. Resuscitation, which included mechanical ventilation, was attempted in 66% of patients. This maintained life for more than a few hours in 22% of cases. Lumbar puncture had preceded the final deterioration in 43%. Of these clinical PE cases, 63% had intracranial hemorrhages in addition to SAH. The mean brain weight was 1442 ± 121 gm, and the mean lung weight was 1490 ± 259 gm. Cerebral edema and herniations were always present. In the clinical PE group, mean initial arterial gas values were: PaO2, 49 ± 10 mm Hg; PaCO2, 32 ± 7 mm Hg; pH, 7.40 ± 0.14; and O2 saturation, 88 ± 0%. Following oxygen therapy the values were: PaO2; 211 ± 91 mm Hg; PaCO2, 24 ± 9 mm Hg; pH, 7.5 ± 0.08; and O2 saturation, 99 ± 1%.

Patients with the most rapid downhill courses were most likely to have PE. Of the patients with clinical PE, 72% died in less than 24 hours; of those with pathological PE, the corresponding figure was 32%, while for those without PE it was only 19%.

More of the patients with pathological PE presented as acute cardiopulmonary catastrophes, and had ventilatory assistance and pulmonary and/or cardiac resuscitation, than those without PE, but the differences did not achieve statistical significance (Table 5).

TABLE 5

Comparison of the therapy attempted in patients with and without pathological diagnosis of pulmonary edema (PE) at autopsy*

TherapyCases With Pathological PE (%)Cases Without Pathological PE (%)
intubation4026
tracheotomy1613
respirator5735
intermittent positive
 pressure breathing209
clipping or coating
 aneurysm2943
decompressive
 craniotomy or
 craniectomy134
evacuation of clot70
CSF drainage
 (external or
 ventriculoatrial
 shunt)54
diuretics2417
attempted cardiac
 resuscitation110

No significant differences (p > 0.05).

Discussion

The dramatic increase in intracranial pressure (ICP) that follows aneurysmal rupture appears to trigger a massive autonomic discharge which causes virtually instantaneous circulatory adjustments. The homeostatic aim of this is to maintain cerebral perfusion but the pathological price paid may be accumulation of water in brain and lung. This review has demonstrated a relatively high incidence of PE following fatal SAH from aneurysmal rupture and the clinical features were consistent with increased sympathetic nervous system activity.

The major physiological abnormalities in PE are a right-to-left shunt and a decrease in lung compliance. Alveoli collapse when fluid fills them, and this leads to a cessation of ventilation, although capillary flow continues and compliance falls.2 The ultimate effect of these processes is hypoxemia. Such hypoxemia was significantly greater in patients who died with pathological PE than those without.

The salient features of neurogenic PE have been summarized as follows: extremely rapid onset, association with hypothalamic injury, suppression by adrenergic blockers or central nervous system depressants, high protein edema fluid, and resemblance to epinephrineinduced PE. The hemodynamic sequence involved vasoconstriction with a shift in blood from the high-pressure systemic to the low-pressure pulmonary system; in association with increased pulmonary capillary pressure this produces a structural pulmonary injury and unbalancing of Starling forces, which causes pulmonary hemorrhage and PE.22 The role of the hypothalamus is questioned by human autopsy studies.5,15 Intracisternal injection or mechanical compression in animals leads to PE which is not prevented by vagotomy, atropine, mid-collicular decerebration or adrenalectomy, although it is ameliorated by stellate-T5 ganglionectomy, sympathetic blocking agents, and C7–8 cord transection.3,19 The physiopathological sequence in the primate has been described by Ducker and Simmons8 as increase in ICP, systemic vasoconstriction, and generalized hypertension. While these hemodynamic adjustments assisted the perfusion of the compressed brain, in 15% to 20% of animals the peripheral resistance rose to extreme levels, cardiac output failed, the left atrium distended, and PE rapidly appeared; pulmonary venous pressure always exceeded pulmonary arterial pressure for some seconds. Malik13 studied pulmonary vascular responses in dogs in which ICP was increased. Pulmonary vascular resistance and pulmonary arterial pressure increased markedly, but there was little change in pulmonary blood flow. Pretreatment with phenoxybenzamine (an α-adrenergic blocker) inhibited the changes. Animals with raised ICP had a drop in mean PaO2 from 90 to 56 mm Hg, but if phenoxybenzamine was given the change was only from 84 to 82 mm Hg. Significantly, it was shown that pulmonary arterial hypertension could occur independently of increases in left atrial pressure. All the hypoxemia observed in our clinical cases could not be explained solely on the basis of shunting, since there was usually a good elevation of PaO2 in response to an increase in inspired oxygen concentration. In a study of SAH in the spontaneously breathing primate, Rothberg, et al.,16 found a reduction in cerebral blood flow and respiratory abnormalities (apnea, irregular respiratory patterns, hyperventilation), which increased with larger volumes of subarachnoid blood. Greater hypoxemia and hypocapnia were associated with increased mortality.16 Similarly, patients in this series who had pathological PE died sooner and had greater hypoxemia and hypocapnia (more hyperventilation) than those without.

The common thread that runs through the reported cases of PE in association with intracranial pathology appears to be the acuteness of the rise in ICP (which is consistent with a high incidence following aneurysmal rupture), and not the absolute level of ICP.7,11 In a series of fatal war injuries, Simmons, et al.,20 described 56 patients of whom only two died with normal lungs. Of those who died in under 7 days, 88% had PE and 12% pneumonia; of those who died after 7 days, 71% had PE and 29% pneumonia. A similar temporal relationship was seen in our cases. Caution in interpreting PE as being the sole result of intracranial pathology when the two are associated was urged by Graf and Rossi.11 Only five of 1700 autopsy cases had clinical PE, and none of these patients died of vascular causes. The occurrence of PE in cord-injured (presumably sympathectomized) patients is intriguing.

In normal man, ventilation is increased by hypercapnia, hypoxemia, and acidemia. A normal 70-kg man (PaCO2 = 40 mm Hg) would increase his ventilation from 6 to over 20 liters/min in the face of a fall in his PaO2 to 48 mm Hg (the mean of the patients in this series with pathological PE).1 In healthy subjects aged 41 to 50 years, the PaO2 averages 83.9 ± 4 mm Hg; in those aged over 60 years it falls to 74.3 ± 4 mm Hg. Corresponding normal PaCO2 values are 39.6 ± 2 and 39.8 ± 2 mm Hg.21 In Edmonton, however, which is 2200 feet above sea level, normal adults have a PaO2 level about 10 mm Hg lower than these values; similarly PaCO2 values are about 5 mm Hg lower. The degree of hyperventilation apparent in our cases, as evidenced by low PaCO2, can mask an increasing alveolar-arterial difference for oxygen, and even an apparently normal PaO2 may not reflect the degree of abnormality in oxygen transport. The initial mechanism of hyperventilation following SAH is probably a central neurogenic stimulation rather than hypoxemia or cerebrospinal fluid acidosis.10,12,18 Following a variety of brain insults, hyperventilation is associated with a poor prognosis.14,17

The arrival of a comatose, cyanotic, gurgling and gasping patient who has collapsed with a severe headache shortly before admission should suggest the diagnosis of ruptured aneurysm and PE. Endotracheal intubation should be carried out to permit mechanical ventilation and suctioning of secretions, to prevent upper airway obstruction and aspiration, and to guarantee the desired inspired oxygen concentration. Positive end-expiratory pressure with the patient in the 30° head-up position can improve oxygenation and increase intracranial compliance.9 It is unnecessary to increase the PaO2 above 100 mm Hg.6 Furosemide and mannitol, through their diuretic actions, can assist both lung and brain. A difficult therapeutic judgment would be the employment of phenoxybenzamine or some other α-blocker. Theoretically, this should help the lungs, but the resultant hypotension might reduce cerebral perfusion, which is probably already critically low. If hyperventilation, ventricular drainage, surgical decompression, clot removal, and/or some other means of reducing ICP were in concurrent use, the judicious use of such drugs in a patient with fulminant PE might be warranted. The use of salt-poor albumen, digitalis, and morphine could be considered.

This study suggests that the barriers to excess water uptake in both brain and lung can be overcome simultaneously in SAH of fatal proportions.

Acknowledgments

I am grateful to Richard L. Jones, Ph.D., and John Hanson, M.Sc., for their helpful criticisms and advice.

References

  • 1.

    Berger AJMitchell RASeveringhaus JW: Regulation of respiration (third of three parts). N Engl J Med 297:1942011977N Engl J Med 297:

  • 2.

    Bushnell LS: Acute respiratory failure in the surgical patient: physiology and managementSkillman JJ (ed): Intensive Care. Boston: Little, Brown and Co1975203227Intensive Care.

  • 3.

    Chen HISun SCChai CY: Pulmonary edema and hemorrhage resulting from cerebral compression. Am J Physiol 224:2232291973Am J Physiol 224:

  • 4.

    Ciongoli AKPoser CM: Pulmonary edema secondary to subarachnoid hemorrhage. Neurology 22:8678701972Neurology 22:

  • 5.

    Crompton MR: The pathogenesis of cerebral infarction following the rupture of cerebral berry aneurysms. Brain 87:4915101964Crompton MR: The pathogenesis of cerebral infarction following the rupture of cerebral berry aneurysms. Brain 87:

  • 6.

    Don HF: Ventilatory managementBerk JLSampliner JEArtz JSet al (eds): Handbook of Critical Care. Boston: Little, Brown and Co197687114Handbook of Critical Care.

  • 7.

    Ducker TB: Increased intracranial pressure and pulmonary edema. Part 1: Clinical study of 11 cases. J Neurosurg 28:1121171968Ducker TB: Increased intracranial pressure and pulmonary edema. Part 1: Clinical study of 11 cases. J Neurosurg 28:

  • 8.

    Ducker TBSimmons RL: Increased intracranial pressure and pulmonary edema. Part 2: The hemodynamic response of dogs and monkeys to increased intracranial pressure. J Neurosurg 28:1181231968J Neurosurg 28:

  • 9.

    Frost EAM: Respiratory problems associated with head trauma. Neurosurgery 1:3003061977Frost EAM: Respiratory problems associated with head trauma. Neurosurgery 1:

  • 10.

    Fujishima MSugi TChoki Jet al: Cerebrospinal fluid and arterial lactate, pyruvate and acid-base balance in patients with intracranial hemorrhages. Stroke 6:7077141975Stroke 6:

  • 11.

    Graf CJRossi NP: Pulmonary edema and the central nervous system: a clinico-pathological study. Surg Neurol 4:3193251975Surg Neurol 4:

  • 12.

    Lane DJRout MWWilliamson DH: Mechanism of hyperventilation in acute cerebrovascular accidents. Br Med J 3:9121971Br Med J 3:

  • 13.

    Malik AB: Pulmonary vascular response to increase in intracranial pressure: role of sympathetic mechanisms. J Appl Physiol 42:3353431977Malik AB: Pulmonary vascular response to increase in intracranial pressure: role of sympathetic mechanisms. J Appl Physiol 42:

  • 14.

    North JBJennett S: Abnormal breathing patterns associated with acute brain damage. Arch Neurol 31:3383441974Arch Neurol 31:

  • 15.

    Richards P: Pulmonary oedema and intracranial lesions. Br Med J 2:83861963Richards P: Pulmonary oedema and intracranial lesions. Br Med J 2:

  • 16.

    Rothberg CSWeir BKAOverton TRet al: The pathophysiology of induced SAH in the spontaneously breathing Cynomolgus monkey using different volumes of fresh autogenous blood. Acta Neurol Scand 56 (Suppl 64):3303311977Acta Neurol Scand 56 (Suppl 64):

  • 17.

    Rout MWLane DJWollner L: Prognosis in acute cerebrovascular accidents in relation to respiratory pattern and blood gas tensions. Br Med J 3:791971Br Med J 3:

  • 18.

    Sambrook MAHutchinson ECAber GM: Metabolic studies in subarachnoid haemorrhage and strokes. I. Serial changes in acid-base values in blood and cerebrospinal fluid. Brain 96:1711901973Brain 96:

  • 19.

    Sarnoff SJSarnoff LC: Neurohemodynamics of pulmonary edema. II. The role of sympathetic pathways in the elevation of pulmonary and systemic vascular pressures following the intracisternal injection of fibrin. Circulation 6:51621952Circulation 6:

  • 20.

    Simmons RLMartin AM JrHeisterkamp CA IIIet al: Respiratory insufficiency in combat casualties. II. Pulmonary edema following head injury. Ann Surg 170:39441969Ann Surg 170:

  • 21.

    Sorbini CAGrassi VSolinas Eet al: Arterial oxygen tension in relation to age in healthy subjects. Respiration 25:3131968Respiration 25:

  • 22.

    Theodore JRobin ED: Speculation on neurogenic pulmonary edema (NPE). Am Rev Respir Dis 113:4054111976Am Rev Respir Dis 113:

  • 23.

    Weisman SJ: Edema and congestion of the lungs resulting from intracranial hemorrhage. Surgery 6:7227291939Weisman SJ: Edema and congestion of the lungs resulting from intracranial hemorrhage. Surgery 6:

Article Information

Address reprint requests to: Bryce K. Weir, M.D., Department of Surgery, 11–102 D Clinical Sciences Building, The University of Alberta, Edmonton, Alberta, Canada T6G 2E1.

© AANS, except where prohibited by US copyright law.

Headings

References

1.

Berger AJMitchell RASeveringhaus JW: Regulation of respiration (third of three parts). N Engl J Med 297:1942011977N Engl J Med 297:

2.

Bushnell LS: Acute respiratory failure in the surgical patient: physiology and managementSkillman JJ (ed): Intensive Care. Boston: Little, Brown and Co1975203227Intensive Care.

3.

Chen HISun SCChai CY: Pulmonary edema and hemorrhage resulting from cerebral compression. Am J Physiol 224:2232291973Am J Physiol 224:

4.

Ciongoli AKPoser CM: Pulmonary edema secondary to subarachnoid hemorrhage. Neurology 22:8678701972Neurology 22:

5.

Crompton MR: The pathogenesis of cerebral infarction following the rupture of cerebral berry aneurysms. Brain 87:4915101964Crompton MR: The pathogenesis of cerebral infarction following the rupture of cerebral berry aneurysms. Brain 87:

6.

Don HF: Ventilatory managementBerk JLSampliner JEArtz JSet al (eds): Handbook of Critical Care. Boston: Little, Brown and Co197687114Handbook of Critical Care.

7.

Ducker TB: Increased intracranial pressure and pulmonary edema. Part 1: Clinical study of 11 cases. J Neurosurg 28:1121171968Ducker TB: Increased intracranial pressure and pulmonary edema. Part 1: Clinical study of 11 cases. J Neurosurg 28:

8.

Ducker TBSimmons RL: Increased intracranial pressure and pulmonary edema. Part 2: The hemodynamic response of dogs and monkeys to increased intracranial pressure. J Neurosurg 28:1181231968J Neurosurg 28:

9.

Frost EAM: Respiratory problems associated with head trauma. Neurosurgery 1:3003061977Frost EAM: Respiratory problems associated with head trauma. Neurosurgery 1:

10.

Fujishima MSugi TChoki Jet al: Cerebrospinal fluid and arterial lactate, pyruvate and acid-base balance in patients with intracranial hemorrhages. Stroke 6:7077141975Stroke 6:

11.

Graf CJRossi NP: Pulmonary edema and the central nervous system: a clinico-pathological study. Surg Neurol 4:3193251975Surg Neurol 4:

12.

Lane DJRout MWWilliamson DH: Mechanism of hyperventilation in acute cerebrovascular accidents. Br Med J 3:9121971Br Med J 3:

13.

Malik AB: Pulmonary vascular response to increase in intracranial pressure: role of sympathetic mechanisms. J Appl Physiol 42:3353431977Malik AB: Pulmonary vascular response to increase in intracranial pressure: role of sympathetic mechanisms. J Appl Physiol 42:

14.

North JBJennett S: Abnormal breathing patterns associated with acute brain damage. Arch Neurol 31:3383441974Arch Neurol 31:

15.

Richards P: Pulmonary oedema and intracranial lesions. Br Med J 2:83861963Richards P: Pulmonary oedema and intracranial lesions. Br Med J 2:

16.

Rothberg CSWeir BKAOverton TRet al: The pathophysiology of induced SAH in the spontaneously breathing Cynomolgus monkey using different volumes of fresh autogenous blood. Acta Neurol Scand 56 (Suppl 64):3303311977Acta Neurol Scand 56 (Suppl 64):

17.

Rout MWLane DJWollner L: Prognosis in acute cerebrovascular accidents in relation to respiratory pattern and blood gas tensions. Br Med J 3:791971Br Med J 3:

18.

Sambrook MAHutchinson ECAber GM: Metabolic studies in subarachnoid haemorrhage and strokes. I. Serial changes in acid-base values in blood and cerebrospinal fluid. Brain 96:1711901973Brain 96:

19.

Sarnoff SJSarnoff LC: Neurohemodynamics of pulmonary edema. II. The role of sympathetic pathways in the elevation of pulmonary and systemic vascular pressures following the intracisternal injection of fibrin. Circulation 6:51621952Circulation 6:

20.

Simmons RLMartin AM JrHeisterkamp CA IIIet al: Respiratory insufficiency in combat casualties. II. Pulmonary edema following head injury. Ann Surg 170:39441969Ann Surg 170:

21.

Sorbini CAGrassi VSolinas Eet al: Arterial oxygen tension in relation to age in healthy subjects. Respiration 25:3131968Respiration 25:

22.

Theodore JRobin ED: Speculation on neurogenic pulmonary edema (NPE). Am Rev Respir Dis 113:4054111976Am Rev Respir Dis 113:

23.

Weisman SJ: Edema and congestion of the lungs resulting from intracranial hemorrhage. Surgery 6:7227291939Weisman SJ: Edema and congestion of the lungs resulting from intracranial hemorrhage. Surgery 6:

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