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Ann Thorac Surg 2006;81:643-648
© 2006 The Society of Thoracic Surgeons

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Original article: Cardiovascular

Differential Distribution of Lipid Microemboli After Cardiac Surgery

^a Department of Cardiothoracic Anesthesiology, Center for Heart and Lung Disease, Lund University Hospital, Lund
^b Department of Cardiothoracic Surgery, Center for Heart and Lung Disease, Lund University Hospital, Lund
^c Department of Clinical Physiology, University Hospital Malmö, Malmö, Sweden

Accepted for publication August 15, 2005.

^_* Address correspondence to Dr Jönsson, Department of Cardiothoracic Surgery, Center for Heart and Lung Disease, Lund University Hospital, SE-221 85 Lund, Sweden (Email: henrik.jonsson{at}med.lu.se).

	Abstract

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
BACKGROUND: Lipid microemboli found in shed blood during cardiac surgery have been shown to block capillaries of the brain postoperatively. In this study, the distribution of lipid microemboli in different regions of the brain and other organs was examined. A novel porcine model using radioactive lipid particles was used.

METHODS: Ten animals (2 controls and 8 cases) were anesthetized and put on cardiopulmonary bypass. A shed-blood phantom was produced from arterial blood, saline, and tritium-labeled triolein. The phantom was infused into the cardiopulmonary bypass circuit. Tissue samples were taken postmortem from examined organs and prepared for scintillation counting. Levels of radioactivity were used as a measure of the uptake of lipid microemboli.

RESULTS: High levels of radioactivity were found in kidney and spleen (5 to 10 times higher than in the other organs investigated). In the brain, radioactivity was found in all regions examined. The gray matter of cerebrum showed the highest level of the regions examined.

CONCLUSIONS: This study shows that embolization of lipids is not a phenomenon restricted to the brain, but affected all the organs examined. The high levels found in the kidneys, and the relatively high levels in the gray matter of the cerebrum further legitimize the debate on the impact lipid microemboli has on postoperative kidney and cognitive dysfunction.

	Introduction

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The practice of retransfusing shed blood during cardiac surgery with cardiopulmonary bypass (CPB) using cardiotomy suction has been shown to be a major source of lipid microemboli (LME) [1–4]. These lipid emboli form small occlusions in the vasculature, and histologic examination of the brain after cardiac surgery has demonstrated lipid deposits in the capillaries in this organ [4]. These phenomenon found in the capillary bed is sometimes referred to as small capillary arteriolar dilatations (SCADS) [4]. In addition, SCADS/LME have been proposed as an important contributor to the postoperative cognitive dysfunction observed in some patients after surgery involving CPB [5, 6].

Until now, attention has been focused on emboli in the brain and the effects they may have on cerebral function. In this study we wanted to investigate whether LME also affect other organs, and if so, the distribution of embolic load to different organs. To achieve this, a novel porcine model employing radioactive LME was used.

	Material and Methods

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After gaining approval from the regional Animal Study Ethics Committee, 10 adult landbred pigs (weight, 66 to 72 kg) were used. Two animals served as controls and 8 animals formed a case group. During the experiment vital measurements, namely, blood pressure, central venous pressure, electrocardiogram, nasopharyngeal temperature, ventilator settings, and pulse oximetry, were monitored continuously. Catheters for monitoring, drug delivery, and blood sampling were inserted into a vein in one of the ears, the jugular internal vein, and the femoral and carotid arteries.

Anesthesia and Perfusion
Premedication was performed with an intramuscular injection of 15 mg/kg ketamine chloride (Ketalar; Pfizer, New York, NY) and 0.2 mg/kg xylasine (Rompun; Bayer, Gothenburg, Sweden). Anesthesia was induced by an intravenous injection of sodium thiopental (Pentothal; Abbot, North Chicago, Illinois) 10 mg/kg and atropine (Atropin Merck NM; Merck NM, Stockholm, Sweden) 0.02 mg/kg. Surgical preparations were made for tracheotomy. After giving an intravenous injection of succinylcholine (Celocurin; Ipex, Solna, Sweden) 0.2 mg/kg to obtain muscle relaxation, the endotracheal tube was inserted. Anesthesia was maintained by infusion of 0.15 mg · kg^–1 · min^–1 ketamine chloride and 0.01 mg · kg^–1 · min^–1 pancuronom bromide (Pavulon; NV Organon, Oss, Netherlands), or by infusion of 0.1 to 0.2 mg · kg^–1 · min^–1 propofol (Diprivan; Astra-Zeneca, Luton, United Kingdom) together with intermittent injections of fentanyl (Leptanal; Lilly, France) and atracuriumbesylate (Janssen-Cilag AB, Sollentuna, Sweden).

The animals were connected to a ventilator and the pCO₂ was maintained at between 4.5 and 6.0 kPa.

A sternotomy was performed to expose the heart, and the right atrium and the ascending aorta were cannulated after a full dose of heparin (LEO Pharma A/S, Copenhagen, Denmark) had been administered. A Jostra HL 15 heart-lung machine (Jostra AB, Lund, Sweden) was used with a Jostra Quadrox oxygenator and Jostra Quart arterial filter. Perfusion was maintained at approximately 2.0 L · m^–2 · min^–1. Cardiopulmonary bypass was instituted as soon as the animal's circulation was stable. All animals underwent standardized perfusion for 40 minutes, and were then weaned from bypass.

Administration of Radio-Labeled Triolein
A solution of radioactive triolein was prepared by mixing a 65% nonradioactive triolein solution (Carl Roth GmbH, Karlsruhe, Germany) with radioactive tritium-labeled triolein (Amersham BioSciences, Little Chalfont, United Kingdom). The proportions used were such that 5 mL of the final solution should contain 1 mCi of radioactivity.

A shed-blood phantom was made by mixing 200 mL blood from the cardiotomy reservoir with 200 mL saline and 5 mL radioactive triolein solution. The shed-blood phantom was gently agitated for approximately 1 minute and retransfused into the cardiotomy reservoir of the heart-lung machine after 20 minutes of bypass. It was allowed to flow into the reservoir as quickly as possibly, normally 30 to 60 seconds. After weaning from CPB, the animals were sacrificed using potassium chloride (Kaliumklorid; B. Braun, Melsungen, Germany) and sodium thiopental.

Sample Preparation
After sacrificing the animals, tissue samples were taken from the white matter of the cerebrum, gray matter of the cerebrum, brainstem, hippocampus, cerebellum, heart, left lung, liver, cortex of one kidney, spleen, small intestine and skeletal muscle. Four tissue samples of 100 to 200 mg were dissected from each investigated organ.

To each sample, 2 mL Soulene 350 (Packard Bioscience, Groningen, Netherlands) was added. The samples were placed in an air heater at 37°C for 24 hours. When the tissue samples had dissolved, 0.2 mL hydrogen peroxide was added to decolorize the samples, and they were then placed in the air heater at 60°C for 30 minutes. An additional 0.2 mL hydrogen peroxide was added. Fifteen milliliters of scintillation fluid (Hionic Fluor; Packard Bioscience) was added, and the samples were then left to stand for 4 to 6 days to allow the chemoluminescence to decrease [7].

The beta radiation from the tritium-labeled triolein was used as a marker for triolein content. The level of radioactivity (beta radiation) was measured by scintillation counting, using a liquid scintillation counter (14814 Win Spectral Guardian; Wallac Oy, Turku, Finland) together with the software supplied by the manufacturer (Easycount). This software automatically excludes background radiation [7]. The specific activity of tritium was calculated for each sample. Two separate measurements were performed for every sample. Radioactivity is reported as the number of disintegrations per minute per gram sample (DPM/g).

Statistics
For each organ, a mean value was determined from the four specimens and the two radioactivity measurements. Values for the control animals and the case group were expressed as mean ± 1 SD, unless otherwise stated. In addition, the radioactivity in each animal was standardized by representing the amount of radioactivity found in each organ or tissue as a percentage of the total radioactivity for the animal (sum of all examined organs or tissues).

To compare radioactivity between different tissues, a t test was performed. To compare differences in radioactivity within different regions of the brain, a repeated-measurement analysis of variance analysis (ANOVA) was performed. A p value less than 0.05 was considered significant.

	Results

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No beta radiation was detected in the tissues of the nonradioactive animals (Table 1). In the radioactive group, beta radiation was detected in all tissues examined indicating the presence of LME. The highest levels of radioactivity were found in samples taken from the kidneys and spleen. The radioactivity in these organs was approximately 5 to 10 times higher than in the other organs examined (Table 1). Liver and the gray matter of the cerebrum showed the third and fourth highest levels of beta radiation, respectively. The lowest levels were found in skeletal muscle. No radiation was detected in venous blood before the shed the blood phantom was added to the circulation. High levels of radioactivity were found in the shed-blood phantom. Just before euthanasia, no radiation was detected in venous blood (Table 1).

View larger version (18K): [in this window] [in a new window]   Fig 2. Relative distribution of radioactivity, shown as the standardized concentration of lipid microemboli in different tissues (levels are expressed as a percent of total radioactivity from all tissues examined for each animal).

The distribution of beta radiation in the regions of the brain examined showed differences that were statistically significant when tested with ANOVA analysis (Table 1). The level of radioactivity found in gray matter of cerebrum was significantly higher than in the other regions of the brain examined (t test, p < 0.05 in all tests). Brainstem showed the significantly lower levels of beta radiation in the brain as compared with grey matter and cerebellum (t test, p < 0.05).

	Comment

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
This study shows that lipid particles introduced into the cardiopulmonary circuit, not only affects the brain, but is a global phenomenon affecting all organs. In addition, the variation from organ to organ is large, with the kidneys, liver, and spleen seeming to have the highest embolic load.

The kidneys were found to be the organ with the highest uptake of LME. Since the kidneys are well-perfused organs [8], it is to be expected that they would receive a relatively large load of LME. However, the extremely high levels found in this study are surprising. In a recent study by Boston and colleagues [9] blood flow to different organs was studied in a porcine model. In their study, which also was performed at normothermia and with the same CPB flow as in our study, they found a higher blood flow to the brain than to the kidneys. In our study, we found nearly a 10-fold higher beta radiation level in the kidneys than in the brain. This finding indicates that it is not only the blood flow to the kidneys that is responsible for the uptake of LME. In the model employed by Boston and associates [9,10], fluorescent microspheres were used which is a validated method for measuring blood flow, whereas in our model we used lipid emboli, which are heterogeneous in size. As with the lipid emboli found in shed human blood, little is known about the distribution in size. However, in the cardiopulmonary circuit, the 40-µm arterial filter will probably break down larger emboli to a size less than 40 µm. It is therefore likely that other factors, such as the morphology of the capillary network play a role, and the double capillary network (glomeruli and tubuli) found in the kidneys may be especially susceptible to lipid microemboli.

A well-known complication after cardiac surgery is renal dysfunction [11]. As this study clearly shows that the kidneys have the greatest uptake of LME, a pertinent question is whether LME are a contributing factor to this complication. At least two different potential mechanisms responsible for organ dysfunction by lipid emboli are possible. Mechanical obstruction is of course one of them. It has been shown in vitro that mediastinal fat clogs filters and impairs circulation [12]. This study shows a high uptake of lipid material in the kidneys, and it is therefore likely that these emboli cause a mechanical obstruction to blood flow. Another explanation could be a toxic reaction. It has been shown that oleic acid, when given intravenously to test animals, causes lung injury with edema and severe hypoxemia [13]. In addition, it has been shown that uncharged fat (such as triglycerides) and also free fatty acids have toxic properties. In a feline model, triolein and oleic acid cause both vasogenic and cytotoxic cerebral edema when infused into the carotid artery [14]. In this study, the charged oleic acid caused the greatest damage. This implies that lipid material can not only cause mechanical obstruction but chemical interactions may also play a negative role in the capillaries of the organs.

The finding of a high uptake of LME in the kidneys together with the well- known problem of a postoperative renal dysfunction is intriguing. However, this study does not address the pathological effects of lipid-microembolism on the kidneys. Therefore, further studies must be undertaken in this area.

The spleen and the liver had the second and third highest uptakes of LME. Both organs are well perfused [8] and therefore expected to receive a high load of LME. Also, the spleen and the liver share the same type of capillary bed, the sinusoidal capillary [15]. This capillary type is complex with apertures communicating with the underlying tissue. This morphologic trait may play a role in trapping LME. It could potentially promote a diffusion of lipids, in this case triolein, to the tissue interstitium. In addition, the liver and the spleen are part of the reticuloendothelial system [16] and contain cells with phagocytic activity, which could actively take up LME. Although a high uptake was found in these organs, the clinical relevance is unclear.

The brain has been the organ of focus in research on LME/SCADS [2, 4], and we therefore expected to find radioactive lipid material in our model, and that was, indeed, the case. At first glance, the overall levels of beta radiation in the brain were lower than anticipated. Compared with kidneys and spleen for example, the levels were only a fraction of these levels, and could therefore be assumed to be of less importance. However, the porcine model used may not be completely representative of the clinical setting. Cerebral blood flow in pigs is somewhat lower than in humans [8–10, 17]. Pigs also have a rete mirabile, which could affect the rate of embolization. This is a vascular rete situated between the carotid arteries and cerebral vessels, which acts a thermoregulator [18]. The small vessels of the rete could work as screen filter for emboli. In addition, histologic differences between capillaries could also be a factor. For instance, spleen and brain have not the same type of capillary bed. The brain has continuous capillaries, whereas spleen has sinusoidal capillaries. This difference could affect the ability to trap LMEs. Yet another important aspect is the auto regulation of cerebral blood flow. That could produce a better wash out of the capillary bed, which would lead to a lesser amount of trapped LME in the brain. To mimic cerebral fat embolism in a rat model, Drew and associates [19] injected radio labeled triolein directly into the carotid artery. They determined the blood flow to the brain, and found that 44% of the injected microspheres where found in the brain, but only 30% of the injected triolein remained in the brain at 30 minutes after injection. They also found that 25% of the triolein in the brain left the brain within 15 minutes. These factors may influence the level of embolization in the model described here, and thus give levels lower than would have been found in humans.

This study corroborates previous findings that lipid microemboli from shed mediastinal blood causes massive microembolization in the brain [2, 4]. The question of the relation between these emboli and the cognitive dysfunction seen after surgery is not addressed in this study. The connection between the two entities is intriguing and have been suggested [5, 6, 20]. Our study did, however, reveal differences between different regions of the brain (Table 1). Low levels were found in the brainstem, for example, and the highest in the gray matter of the cerebrum. These differences are probably due to differences in blood flow in different regions, but histologic aspects in different regions could also play a part in the trapping of emboli. One interesting observation is that we found the highest levels in the gray matter of the cerebrum, which is involved in cognitive functions of the brain [21]. This finding will further spur the debate on the possible relation between LME and postoperative cognitive dysfunction.

In all, our findings clearly show that LME are unevenly dispersed in different parts of the brain, and there is no evidence that any region is spared from embolization.

The levels of radioactivity found in the heart, small intestine, and skeletal muscle were low. These finding could be anticipated, as blood flow, through, for instance, skeletal muscle, is significantly reduced during CPB [9, 10]. The low uptake in the heart could be explained by the fact that the cardiac output performed by the heart was low. That will lower the metabolism in the heart and reduce the blood flow in the coronary artery.

The radioactivity found in the lungs was higher than expected. One possible explanation is that the pulmonary circulation was not entirely bypassed as we did not cross-clamp the ascending aorta. As a consequence, the heart was beating with small stroke volumes during the experiment. Thus, some blood circulated through the lungs, and an uptake of emboli could occur. In addition, the bronchial circulation could have contributed to the uptake. Finally, the lungs are a part of the immune system. Leukocytes that have phagocytized lipid material can adhere to pulmonary capillaries and in this way contribute to the uptake of radio labeled triolein. As the lung circulation is situated after the capillary bed in the systemic circulation, the high uptake in the lungs suggests recirculation of LME.

By using a radioactive method employing beta radiation to study these emboli, we found a model with which to follow the differential distribution in detail and which gave reproducible results. However, this method is not without difficulties. Firstly, radioactive contamination of samples during and after experiments is an issue that must be taken into consideration when performing experiment. For instance, great caution must be taken not to inflict any contamination from samples with higher radioactivity to samples with lower radioactivity. Secondly, isotope must be prepared carefully. In the first animals, high variation from animal to animal was observed. This gave us the lesson to stir the isotope thoroughly before retransfusion. Thirdly, we can not be sure that the content in our shed-blood phantom exactly mimics shed mediastinal blood seen in the cardiotomy suction blood during bypass. Triolein has been used in several studies before with aim to study lipid embolization to lung and brain [14, 19, 22, 23]. In addition, triolein consists of three oleic acid chains and oleic acid is the most common one of the fatty acids seen in adipose tissue in the human body [24] (Table 2). Moreover, due to the double bond of oleic acid, the triglyceride has a low melting point (5.0°C) and will flow freely into and in the shed blood. In the surgical field in humans, triglycerides in liquid phase are probably those ending up in the blood, forming LME. The size and shape of the lipid emboli formed in blood depend on several factors. Probably temperature, hematocrit, presence of lipoprotein, and other proteins are among those factors. In all, several factors support triolein as the lipid of choice. In Figure 1 we can see that the lipid droplets show the same pattern in the blood phantom as in real shed blood. Fourthly, there is always background radiation, which will affect the results. However, with a high dose of radioactivity and software that excludes the background radiation, the impact of background radiation was negligible in this study. Finally, different tissues have different counting efficacies at scintillation counting [7]. However, the examined organs were all in the same range in terms of counting efficacies, and therefore levels are comparable. In summary, the presented porcine model used here with radioactive triolein seems to be a reliable method for tracking lipid emboli and determining the differential distribution throughout the body.

View larger version (122K): [in this window] [in a new window]   Fig 1. (A) Macrophotograph of human shed blood from the surgical field containing triglycerides. (B) Macrophotograph of porcine blood with radioactive triglyceride added.

In conclusion, the study questions the plausibility of routinely retransfusing shed mediastinal blood containing lipid micro particles, which will end up as emboli in different organs. Until evidence exists that these emboli are harmless, maybe it should be assumed that these emboli could be harmful, and care taken to avoid them.

	Acknowledgments

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 
We wish to express our gratitude to Professor Bertil Persson and Gustaf Grafström at the Department of Radiation Physics, Lund University Hospital, for helping us with the isotopes, and to Lars-Erik Nilsson at the Department of Clinical Physiology in Malmö, for providing us with technical assistance and software for scintillation counting. This study was supported by the Swedish Heart-Lung Foundation together with the Crafoord Foundation.

	References

Top Abstract Introduction Material and Methods Results Comment Acknowledgments References

 

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Henrik Jönsson Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Brondén, B. Articles by Jönsson, H. Search for Related Content PubMed PubMed Citation Articles by Brondén, B. Articles by Jönsson, H. Related Collections Extracorporeal circulation