Original Article
Brief Report
Fulminating Fat Embolism Syndrome Caused by Paradoxical Embolism through a Patent Foramen Ovale
N Engl J Med 1993; 329:926-929September 23, 1993
- Article
The post-traumatic fat embolism syndrome is a multisystem disorder characterized by pulmonary and neurologic dysfunction, pyrexia, and a petechial rash1-4. More than a century after the first descriptions of the fat embolism syndrome, the cause of fat emboli and the pathogenesis of the systemic manifestations of this disorder remain incompletely understood. We describe a patient undergoing treatment of a femoral fracture in whom massive fat embolism was demonstrated by transesophageal echocardiography. Acute cor pulmonale developed, precipitating paradoxical fat embolism across a patent foramen ovale, with the subsequent development of the fat embolism syndrome. Embolism of fat across a patent foramen ovale is a possible mechanism responsible for the systemic features of fat embolism syndrome.
Case Report
A 79-year-old man was admitted after a fall resulting in a closed fracture of the right femoral shaft. He had had a myocardial infarction one year earlier and had made an uncomplicated recovery from an avulsion fracture of the right lesser trochanter two years earlier. The results of laboratory investigations were normal, and the electrocardiogram demonstrated a minor intraventricular conduction defect and no Q waves.
A decision was made to treat the fracture by closed reduction and fixation with an intramedullary nail. The patient received subcutaneous heparin preoperatively and remained well until elective surgery on the 11th day after the injury. Anesthesia was induced with propofol and pancuronium, and after endotracheal intubation the patient was given mechanical ventilation with oxygen, enflurane, and nitrous oxide. The electrocardiogram, oxygen saturation, and end-tidal partial pressure of carbon dioxide were monitored continuously, and a transesophageal echocardiographic probe was introduced to monitor cardiac function. Immediately before surgery the blood pressure was 152/80 mm Hg, the electrocardiogram showed sinus rhythm, the oxygen saturation was 98 percent, and the end-tidal partial pressure of carbon dioxide was 28.5 mm Hg. Transesophageal echocardiography revealed normal left ventricular function with no regional wall-motion abnormality, trivial mitral incompetence, and an enlarged right atrium and coronary sinus. Moderately severe tricuspid regurgitation was present, and the pulmonary-artery systolic pressure was estimated to be 45 mm Hg when the continuous-wave Doppler capabilities of the transesophageal echocardiographic probe were used5. There was no evidence of an atrial septal defect, and the fossa ovalis was identified and appeared intact, with no displacement during the respiratory cycle. No interatrial shunting was identified with color-flow Doppler techniques. Before surgery, no abnormal masses or echogenic material was seen within the heart chambers.
Transesophageal echocardiographic monitoring was performed continuously and recorded on videotape. Several seconds after the insertion of a guide wire into the medullary cavity, a shower of small (1 to 2 mm) echogenic masses appeared within the right atrium and right ventricle. No masses were seen within the left atrium or left ventricle, and there were no changes in physiologic measurements. Manipulation of the medullary cavity resulted in a large increase in the quantity of echogenic material, with complete opacification of the right atrium and the right ventricle (Figure 1Figure 1
Transesophageal Echocardiographic Four-Chamber View, Showing Multiple Fat Emboli in the Right Atrium (RA) and Right Ventricle (RV) during Intramedullary Manipulation.). Among the mass of smaller echoes were numerous highly echogenic bodies, 1 cm in diameter and 1 to 7 cm long. These masses could be seen coiling within the right atrium, sometimes rebounding from the closed tricuspid valve, and often persisting for several cardiac cycles before passing into the right ventricle and the pulmonary artery (Figure 2Figure 2
Transesophageal Echocardiographic Four-Chamber View, Showing a Large Fat Embolus (Arrow) among Smaller Echogenic Masses in the Right Atrium.). Complete opacification of the right heart chambers persisted, and after 60 seconds the interatrial septum was observed to bulge into the left atrium and the flap valve of the fossa ovalis opened, with large quantities of embolic material passing into the left atrium (Figure 3Figure 3
Transesophageal Echocardiographic View of the Interatrial Septum.). Initially, the septal movements occurred in synchrony with the ventilatory cycle, but after a few minutes the septum became persistently displaced, and color-flow mapping confirmed the presence of a right-to-left shunt across the fossa ovalis. Medullary manipulation was halted, but paradoxical embolism continued for a further 20 minutes, and numerous embolic masses as large as 1 cm in diameter could be seen within the heart and aorta. During this period the oxygen saturation decreased to 75 percent, the end-tidal partial pressure of carbon dioxide to 9 mm Hg, and the arterial blood pressure to 72/40 mm Hg. Transesophageal echocardiography demonstrated dyskinesia of the interventricular septum, right ventricular dilatation, and severe tricuspid incompetence, and the estimated pulmonary-artery systolic pressure increased to 80 mm Hg. There was a self-limiting episode of ventricular tachycardia. The patient was resuscitated, and the procedure was completed with the insertion of an intramedullary nail. The nailing was accompanied by the appearance of large quantities of embolic material within all four cardiac chambers.The patient was admitted to the intensive care unit, and a Swan-Ganz catheter was inserted. The pulmonary and systemic vascular resistances were elevated (to 1350 and 5301 dyn • sec • cm-5 per square meter of body-surface area, respectively), and the cardiac index was reduced (to 1.6 liters per minute per square meter). Mechanical ventilation was continued, and inotropic drug therapy was begun for persistent hypotension and oliguria (5 to 20 μg of dobutamine per kilogram of body weight per minute and 4 μg of dopamine per kilogram per minute). The electrocardiogram revealed nonspecific ST-segment and T-wave changes. Measurement of arterial-blood gases during ventilation with 50 percent oxygen revealed a pH of 7.39, a partial pressure of oxygen of 75 mm Hg, and a partial pressure of carbon dioxide of 31.5 mm Hg. The patient remained comatose, and neurologic examination revealed lower-limb hyperreflexia and bilateral extensor plantar responses. Three hours postoperatively, several generalized convulsions were treated with an infusion of phenytoin (loading dose, 10 mg per kilogram). A right-sided subconjunctival hemorrhage and scattered petechial hemorrhages appeared on the trunk and upper arms 18 hours postoperatively. Progressive arterial hypoxemia developed (partial pressure of oxygen, 59.5 mm Hg) despite an inspired oxygen concentration of 100 percent, and the chest film demonstrated bilateral pulmonary infiltrates. The cardiac index fell to 1.2 liters per minute per square meter and did not increase in response to increased doses of dobutamine (20 to 70 μg per kilogram per minute). The patient's oliguria continued, and he died of cardiac and respiratory failure 32 hours postoperatively.
Postmortem examination confirmed the diagnosis of fat embolism syndrome. Scattered petechial hemorrhages were found affecting the pericardium, the skin, and the interlobar fissures of both lungs. Microscopical examination revealed widespread microvascular occlusion by fat emboli, particularly within the lungs (Figure 4Figure 4
Autopsy Specimen of the Lung.), kidney, myocardium, and brain, with evidence of infarction in the cerebrum, cerebellum, and brain stem. Examination of the heart revealed a patent foramen ovale, with a maximal aperture of 0.5 cm. There was dilatation of the tricuspid-valve ring that was consistent with right ventricular failure, and there was subendocardial fibrosis compatible with previous myocardial infarction. Bone specimens taken during manipulation and from the fracture site revealed widespread immature mesenchymal cells within the intertrabecular spaces that were consistent with early healing of the fracture. There was no evidence of deep-vein thrombosis or pulmonary thromboembolism.Discussion
The fat embolism syndrome is an uncommon but well-described complication of skeletal trauma characterized by both pulmonary and systemic fat embolism1-4. Incomplete forms are common, and the spectrum of the fat embolism syndrome includes subclinical, mild, and fulminating presentations6,7. Our patient had a fulminating fat embolism syndrome that met Gurd's three major diagnostic criteria: a petechial rash, respiratory distress, and cerebral signs8. The origin of fat emboli has been debated since the original accounts of the syndrome in the late 19th century. The mechanical theory proposes that intramedullary veins are damaged by trauma, allowing marrow fat to intravasate and embolize to the lungs2. In contrast, the biochemical hypothesis suggests that fat emboli are composed of aggregated chylomicrons and very-low-density lipoproteins that coalesce within the vasculature after trauma, with the formation of fat macroglobules9-11. In our patient, the close temporal association between medullary manipulation and intracardiac embolism is consistent with the mechanical theory of fat embolism. Intramedullary pressure is increased by manipulation and nailing procedures, and these may have promoted the entry of marrow fat into medullary veins. Although the echogenic masses seen inside the heart were not sampled at the moment of embolism, subsequent histologic studies showed widespread pulmonary and systemic intravascular fat deposition consistent with fat embolism. These echocardiographic observations are also consistent with those of an experimental study that demonstrated the presence of marrow fat in the femoral vein within seconds of intramedullary manipulation12.
Peltier has proposed that the fat embolism syndrome is primarily a pulmonary disease and has emphasized the importance of increased pulmonary vascular resistance due to widespread microvascular occlusion2. Massive fat embolism obstructs the pulmonary circulation and leads to hypoxemia as a result of ventilation-perfusion inequality. Rapid deterioration may occur, with death from acute right ventricular failure. Our findings are consistent with this hypothesis. Transesophageal echocardiography demonstrated severe and prolonged embolization that resulted in increased pulmonary-artery pressure and pulmonary vascular resistance, right ventricular dilatation, and worsening tricuspid incompetence. The delayed appearance of a petechial rash, neurologic dysfunction, and the development of progressive pulmonary dysfunction are characteristic of the fat embolism syndrome and are consistent with the theory of a secondary phase of tissue damage, possibly due to the toxic effects of free fatty acids liberated by the hydrolysis of fat emboli in the lungs13,14. Histologic examination of patients with systemic fat embolism syndrome typically reveals widespread microvascular occlusion by fat emboli15. Such emboli are believed to reach the systemic circulation either through pulmonary-precapillary shunts or directly across the pulmonary-capillary bed1,16,17. Paradoxical embolism of air and thrombus across a patent foramen ovale is well recognized, but the passage of fat is an alternative mechanism responsible for the systemic manifestations of the fat embolism syndrome. Shunting across a patent foramen ovale can occur during coughing, after the release phase of the Valsalva maneuver, and during mechanical ventilation,18-20 and paradoxical thromboembolism has occurred in pulmonary embolism, chronic lung disease, and right ventricular failure21,22. In this case paradoxical embolism was precipitated by increased right atrial pressure due to acute cor pulmonale. The observation of phasic displacement of the fossa ovalis with the ventilatory cycle suggests that the use of mechanical ventilation may have contributed to this process by cyclic increases in right atrial pressure. The fact that fat is readily deformable accounts for the passage of masses larger than the diameter of the patent foramen ovale17. The foramen ovale is patent in 20 to 34 percent of people,23 and the possibility that this route might be involved in the pathogenesis of the systemic manifestations of the fat embolism syndrome was considered by Sevitt17. In an early study of 24 subjects with systemic fat embolism, none had evidence of an atrial septal defect at autopsy,24 but it is not clear whether patency of the foramen ovale was examined in this series. A right-to-left shunt through a patent foramen ovale was detected with color-flow Doppler techniques in only one of six subjects who had recovered from post-traumatic fat embolism syndrome25. However, the importance of these findings is uncertain, because more recent work indicates that both color-flow Doppler and contrast echocardiography are required to exclude the possibility of patency of the foramen ovale26.
Increasingly, transesophageal echocardiography is used to monitor perioperative cardiac function in patients at high risk. In our experience, echocardiographically detectable fat embolism may be observed in approximately 40 percent of patients undergoing major orthopedic procedures27. At present, routine echocardiographic monitoring cannot be recommended, but future research may provide guidelines for using transesophageal echocardiography and for terminating procedures if evidence of marked embolization is found.
Presented in part at the 42nd annual scientific session of the American College of Cardiology, Anaheim, Calif., March 14-18, 1993.
Dr. Pell is the recipient of a fellowship from the Faculty of Medicine of the University of Edinburgh. Dr. Sutherland holds a Senior Research Fellowship from the British Heart Foundation.
We are indebted to the coroner (Procurator Fiscal), on behalf of whom the postmortem examination was performed, for permission to report the details of this case.
Source Information
From the Departments of Cardiology (A.C.H.P., G.R.S.), Pathology (D.H., A.B.), and Orthopaedic Surgery (J.K., J.C.), Royal Infirmary, Edinburgh, United Kingdom.
Address reprint requests to Dr. Pell at the Department of Cardiology, Western Infirmary, Glasgow G11 6NT, United Kingdom.
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