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Anesthesiology:
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Acute Brain Fat Embolization Occurring after Total Hip Arthroplasty in the Absence of a Patent Foramen Ovale

Colonna, David M. M.D.*; Kilgus, Douglas Ph.D.†; Brown, William Ph.D.‡; Challa, Venkata M.D.§; Stump, David A. Ph.D.∥; Moody, Dixon M. M.D.#

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DURING total joint arthroplasty, showers of bony spicules, marrow fat, and clot are carried by venous blood to the lungs 1; conditions not unlike those present in patients who have suffered traumatic long bone fractures. Like the fat embolism syndrome, which often has a component of neurologic dysfunction, there is recent evidence that total joint arthroplasty and femoral nailing are associated with intraoperative brain embolization as determined by transcranial Doppler ultrasonography 2–4 and magnetic resonance brain imaging. 5 While there are good data demonstrating that intraoperative brain embolization occurs during total joint arthroplasties, the makeup, and even more importantly, the clinical significance of these emboli remain speculative. The authors describe a case of acute brain embolization that occurred in an adult woman undergoing a total hip arthroplasty.
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Case Report

A 77-yr-old, 68-kg woman with chronic lymphocytic anemia, emphysema, hypothyroidism, and gastroesophageal reflux disease fell in her home and suffered a left periprosthetic femur fracture 2 days before she was admitted to the hospital. A transthoracic echocardiogram performed 4 yr before this admission did not demonstrate a patent foramen ovale, although no specific maneuvers were done to diagnose septal defects (e.g., a bubble test). Because of chest pain complaints 3 yr before this current admission, a cardiac catheterization was performed that revealed mild, nonobstructive atherosclerotic coronary artery disease, normal left ventricular wall motion with a 59% ejection fraction, and normal valvular function.
On the morning of surgery, noninvasive monitors were applied, intravenous access was obtained, and a radial artery catheter was inserted. A spinal anesthetic was performed with intrathecal bupivacaine plus epinephrine and fentanyl. After the block was placed, the patient's blood pressure gradually fell from 142/75 mmHg to 108/69 mmHg during 30 min. Thirty minutes after the incision (and approximately 1 h after injection of bupivacaine), methyl methacrylate cement was injected into the femoral canal, immediately followed by the insertion of a stemmed femoral prosthesis. Six minutes later, the patient abruptly developed severe bradycardia to a heart rate of 35 beats/min. She rapidly lost consciousness and was pulseless. She was immediately intubated, and chest compressions were begun. After 35 min of chest compressions and epinephrine administration, she was successfully defibrillated, but she required a continuous epinephrine infusion to support her blood pressure. Her hip wound was rapidly sutured at that point.
An intraoperative, transesophageal echocardiogram was then performed, demonstrating marked right-ventricular dilation, and an underfilled left ventricle with poor contractility. Echogenic material was observed in both ventricles and in the aortic arch. The intracardiac echogenic material did not have the highly reflective appearance that is usually typical of air. No septal defects were noted. The patient remained intubated and was sent to the intensive care unit, where she became progressively hypotensive. Her pupils remained fixed and dilated, and she died approximately 3 h 45 min after her initial cardiac arrest in the operating room.
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An autopsy revealed multiple fat emboli to the lungs with giant cell reaction and fat embolization to the brain, kidney, and heart, when the tissues were treated with a neutral fat stain for microscopic examination. Furthermore, fat globules were noted in postcapillary pulmonary venules, suggesting that fat traversed the pulmonary circulation during the 3 to 4 h elapsed from the time of femoral cement introduction to the time of her death. Acute coronary artery occlusions were not observed, nor was a patent foramen ovale present. On gross examination, the brain was swollen and the gyri somewhat flattened. Portions of the brain were embedded in celloidin, sectioned 100 μm-thick, and alkaline phosphatase enzyme histochemistry was employed for microscopic examination of the cerebral vasculature. 6 Examinations revealed elongated, sausage-shaped emboli, presumably triglycerides or neutral fat, in the small capillaries and arterioles of this woman's brain (Fig. 1). After hand-counting the emboli in multiple, representative, microscopic frames, this brain section was extrapolated to contain approximately 5,000 emboli/cm3.
In summary, this patient had acute cardiac arrest during a cemented repair of a periprosthetic hip fracture. After 35 min of cardiopulmonary resuscitation, a cardiac rhythm was successfully reinstated. Unfortunately, the patient died a little over 3 h later. Her autopsy revealed systemic fat embolization with an extraordinary degree of emboli counted within the brain, despite the absence of a patent foramen ovale.
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Discussion

This case is instructive for two reasons. First, recent data suggest that brain embolization occurs in 40–60% of patients during total joint arthroplasty, 2–4 though the structural nature of the emboli and the degree to which the brain is embolized are unknown. This report is unique in its presentation of human brain specimens, demonstrating extensive brain fat embolization acutely after cemented total joint arthroplasty. There was no evidence of cement or blood clot microembolization in this patient. Second, though several case reports have clearly shown that paradoxical brain fat embolism can occur in the setting of long bone fractures and joint arthroplasties in patients who have patent foramen ovales, 7–9 it is unclear whether clinically significant brain fat embolism occurs in patients who do not have patent foramen ovales. This report suggests that large numbers of fat emboli are able to rapidly traverse the pulmonary circulation (in less than 4 h) in the setting of total hip arthroplasty, even in the absence of a patent foramen ovale. This is supported experimentally in a study using a dog model of femoral pressurization, 10 mimicking femoral nailing in humans, which revealed that systemic fat embolization occurred within 3 h after femoral fat release. This suggests that, at least in dogs, fat emboli in large numbers are able to traverse the lungs rapidly after release from femoral marrow. A recent clinical case report by Byrick et al.5 supports this laboratory finding. This case report told of a woman who had prolonged coma and magnetic resonance imaging findings compatible with brain embolization after undergoing nailing of a femoral shaft fracture, despite the absence of a patent foramen ovale.
Except in the aforementioned dog study, little is known about the histopathologic characteristics of the brain emboli found in a patient after femoral prosthesis insertion. This case report is unique in demonstrating the lipid nature of such brain emboli. Of interest, the brain emboli found in the patient described in this case report appear to be identical to those observed in brain specimens from nonsurvivors of cardiopulmonary bypass. These emboli have been named small capillary arteriolar dilatations (SCADs). 11 The large number of SCADs counted in this patient's brain (approximately 5000/cm3) is greater than the number of cerebral fat emboli found in each of the brains of 54 cardiopulmonary bypass nonsurvivors. 11
We believe that brain embolism during total joint arthroplasties has clinical importance, because of our suspicion that it may underlie postoperative delirium (also referred to as confusional states or cognitive dysfunction). This condition is common in the elderly, occurring in 10–15% of general surgery patients, and in as many as 44–55% in particular subgroups of orthopaedic surgery patients. 12–13 Elderly patients with femoral neck fractures comprise the patient group at greatest risk for postoperative delirium, possibly because of their advanced age and their higher incidence of preoperative cognitive dysfunction. 13 Postoperative confusion is associated with a four-fold increase in the duration of hospital stay after hip fracture surgery. 14 It remains unproven why orthopaedic surgery patients may be at greater risk for postoperative cognitive dysfunction. One testable hypothesis is that some orthopaedic surgeries routinely produce brain embolism (e.g., femoral nailing, hip arthroplasties), causing postoperative cognitive dysfunction. Consistent with this thesis, a recent series of 5 patients described in the journal Stroke revealed that neurologic dysfunction occurred after long bone fractures and was associated with brain microembolism, as detected by transcranial Doppler. 15
In summary, our patient illustrates that brain lipid embolization can occur acutely after insertion of a cemented femoral stem, as shown by the intraoperative transesophageal echocardiography (TEE), even in the absence of cardiac septal defects. In addition, the lipid emboli appear microscopically identical to SCADs, the pathologic brain lesions found in nonsurvivors of cardiopulmonary bypass. 11 The identification of fat emboli within this patient's brain raises many important questions, such as, what is the true incidence of systemic (brain) fat embolization in orthopaedic surgery patients? What is the prognostic importance of lipid brain embolization? What patient subgroups are most susceptible to cognitive dysfunction after brain embolization during orthopaedic surgery? Specifically, are patients with cardiac septal defects at greater risk for brain embolization during orthopaedic surgery? 7–9 Are there differences in brain embolization rates between patients who have cemented versus uncemented prostheses? Further study is warranted.
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References

1. Capan LM, Miller SM, Patel KP: Fat embolism. Anesthesiol Clin North Am 1993; 11: 25–54

2. Sulek CA, Davies LK, Enneking FK, Gearen PA, Lobato EB: Cerebral microembolism diagnosed by transcranial Doppler during total knee arthroplasty: Correlation with transesophageal echocardiography. A nesthesiology 1999; 91: 672–6

3. Edmonds CR, Barbut D, Hager D, Sharrock NE: Intraoperative cerebral arterial embolization during total hip arthroplasty. A nesthesiology 2000; 93: 315–8

4. Colonna DM, Stump DA, Kilgus DJ, Manuel JC, Hilbawi HR: Total hip arthroplasty produces intraoperative brain embolization and neuropsychologic dysfunction up to 6 weeks postoperatively. A nesthesiology 1999; 91: A79

5. Byrick RJ, Korley RE, McKee MD, Schemitsch EH: Prolonged coma after unreamed, locked nailing of femoral shaft fracture. A nesthesiology 2001; 94: 163–5

6. Bell MA, Scarrow WG: Staining for microvascular alkaline phosphatase in thick celloidin sections of nervous tissue: Morphometric and pathological applications. Microvasc Res 1984; 27: 189–203

7. Della Valle CJ, Jazrawi LM, Di Cesare PE, Steiger DJ: Paradoxical cerebral embolism complicating a major orthopaedic operation: A report of two cases. J Bone Joint Surg Am Vol 1999; 81: 108–10

8. Weiss SJ, Cheung AT, Stecker MM, Garino JP, Hughes JE, Murphy FL: Fatal paradoxical cerebral embolization during bilateral knee arthroplasty. A nesthesiology 1996; 84: 721–3

9. Pell AC, Hughes D, Keating J, Christie J, Busuttil A, Sutherland GR: Brief report: fulminating fat embolism syndrome caused by paradoxical embolism through a patent foramen ovale. N Engl J Med 1993; 329: 926–9

10. Byrick RJ, Mullen JB, Mazer CD, Guest CB: Transpulmonary systemic fat embolism. Studies in mongrel dogs after cemented arthroplasty. Am J Respir Crit Care Med 1994; 150: 1416–22

11. Brown WR, Moody DM, Challa VR: Cerebral fat embolism from cardiopulmonary bypass. J Neuropathol Exp Neurol 1999; 58: 109–19

12. Fisher BW, Flowerdew G: A simple model for predicting postoperative delirium in older patients undergoing elective orthopedic surgery. J Am Geriatr Soc 1995; 43: 175–8

13. Lipowski ZJ: Delirium in the elderly patient. N Engl J Med 1998; 578–82

14. Berggren D, Gustafson Y, Eriksson B, Bucht G, Hansson LI, Reiz S, Winblad B: Postoperative confusion after anesthesia in elderly patients with femoral neck fractures. Anesth Analg 1987; 66: 497–504

15. Forteza AM, Koch S, Romano JG, Zych G, Bustillo IC, Duncan RC, Babikian VL: Transcranial doppler detection of fat emboli. Stroke 1999; 30: 2687–2691

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