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Ann Thorac Surg 1999;68:2225-2230
© 1999 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Can technetium 99m pyrophosphate be used to quantify myocardial injury in donor hearts?

Christopher M.R. Satur, FRCS, David Doyle, MD, Sally Darracott-Cankovic, PhD, William Martin, PhD, David J. Wheatley, FRCS

a Department of Cardiothoracic Surgery and Nuclear Cardiology, Glasgow Royal Infirmary, Glasgow, Scotland, United Kingdom

Address reprint requests to Dr Satur, Department of Cardiac Surgery, Queen Elizabeth Hospital, Edgbaston, Birmingham, UK


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. There are no prospective methods available to quantify the myocyte injury in hearts prior to transplantation. The potential of the isotope labeled infarct marker 99m Technetium pyrophosphate (TcPPT) being used in this role was investigated.

Methods. Brain death was induced by creating an extradural space occupying lesion in young adult swine after which hemodynamic changes were monitored and myocyte injury was quantified by histochemistry. TcPPT was administered 5 hours after induction of intracranial hypertension, and after hearts were harvested myocardial uptake was measured. These latter measurements were related to the histochemical assessment of myocyte injury.

Results. Sham animals (n = 4) maintained cardiovascular stability and experienced minimal myocyte injury, grades 0 to 3. BD animals (n = 10) exhibited varying patterns of hemodynamic change and myocyte injury, the latter was significant in 6, graded 4 to 11, p less than 0.05. Uptake of TcPPT by BD hearts was greater than twice the 90th centile sham value in 6. The sensitivity and specificity of greater uptake indicating the presence of myocyte injury was 83.3% and 75% respectively.

Conclusions. TcPPT has the potential to quantify myocardial injury induced by brain death and its potential utility merits further investigation.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Hearts are selected for transplantation by the identification of donors that have cardiovascular stability and do not require the infusion of significant doses of catecholamine. Actuarial mortality after transplantation approximates 20% at 1 year and some authors have suggested that this early mortality and longer term mortality is greater in hearts with evidence of injury prior to transplantation [1–3].

Pathological processes responsible for causing myocyte injury during brain death include an autonomic surge, the "Cushing reflex", that accompanies intracranial hypertension [4, 5]. The cause of intracerebral injury which induces intracranial hypertension and determines the pattern of Cushing response in turn influences the severity of myocyte injury and necrosis [6]. Chronic intracranial space occupying lesions which cause steady and prolonged onset of intracranial hypertension induce a greater Cushing reflex and myocytolysis than processes which are acute and extreme causing rapid destruction of the brain. Hearts obtained from the latter therefore appear to have improved long term prognosis [7]. There is at present no prospective and rapid test available to quantify and distinguish the severity of myocyte injury in donor hearts.

The infarct marker 99m Technetium Pyrophosphate [TcPPT] has been extensively utilized in the diagnosis of acute myocardial infarction and quantification of its size [8]. It is rapidly absorbed from blood by injured myocardium, and the level of uptake has been shown to have a high sensitivity and specificity for diagnosis of ischemic necrosis. 99m Technetium has a sufficiently high rate of particle emission to ensure rapid data collection by a scintillation counter. We therefore sought to evaluate whether this agent would target myocardium of hearts injured by brain death.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Experimental protocol
Adult male Landrace swine weighing a median 27 kg (range 20 to 36 kg) were submitted to a standard anesthetic protocol including premedication and general anesthesia [9]. Following the institution of artificial ventilation, the following were monitored continuously; the electrocardiogram (ECG), the systemic and pulmonary arterial, right and left atrial hydrostatic pressures. Cardiac output was measured with a thermodilution catheter situated in the pulmonary artery. Dual channel bipolar electroencephalogram (EEG) recordings were obtained through intradermal electrodes. An intracranial balloon catheter (ICB) was situated in the extradural space. 5% dextrose solution was infused at a rate of 150 ml/hr and blood losses were replaced with synthetic colloid, Gelofusine solution (Vifor UK Ltd, Chester, UK). Dobutamine hydrochloride was infused to maintain a systolic arterial pressure greater than 80 mm Hg, but was only administered in doses to a maximum 5 mcg/kg/min.

Full preparation was instituted in all animals that had brain death (BD) induced, but in sham animals the ICB was not inserted. Brain death was induced by the inflation of the ICB with water according to the method previously described [9]. These manipulations caused the EEG to become isoelectric and induced variable patterns of hemodynamic change.

Samples of myocardium were obtained from the untraumatized myocardium at the apex of the left ventricle with a Tru-cut biopsy needle (Baxter Healthcare Corporation, Valencia, CA), at baseline and at hourly intervals after induction of intracranial hypertension. They were rapidly chilled in isopentane previously cooled in liquid nitrogen and stored at -70°C until histological evaluation.

Animals were maintained a maximum of six hours after the onset of intracranial hypertension. A median dose of TcPPT of 570 MBq (range 400 to 800 MBq), standardized in a Pitman Radioisotope Calibrator was prepared in 4 ml of saline and was administered 5 hours after the induction of brain death, and a 1/10th sample reserved for gamma camera calibration. If the animal had demonstrated characteristics of premature deterioration TcPPT was administered early. The procedure was terminated by intravenous administration of a hyperkalemic solution to cause rapid cardiac arrest. Hearts were explanted after cardiac arrest and prepared for the evaluation of isotope uptake.

Measurement of creatine kinase
The concentration of creatine kinase and its isoforms were measured in blood samples obtained at baseline, 1 hour after intracranial hypertension and at the termination of the experiment. Serum was prepared and the isoenzymes separated by electrophoresis on an agarose plate. The enzymes were stained and the content measured by densitometry.

Histochemistry
Histochemical evaluation constituted the measurement of the activity the three enzymes succinate dehydrogenase (SDH), monoamine oxidase (MAO) and myosin ATPase [10–12]. 10u sections of the samples were cut on cryotome previously cooled to -30°C and were stained by the methods previously described by Darracott-Cankovic.

Evaluation of samples was performed by a single experienced observer blinded to the identity of samples. The quality of the enzyme activity and distribution was evaluated using a semi-quantitative grading scoring system [11], and grades 0 to 4 were awarded, 0 representing normal quality and 4 poor quality. Grouped statistical analysis compared values for each test and their summated values.

Evaluation of myocardial uptake of TcPPT
Following termination of the experiment and cardiac explantation, all blood was washed from the surface of the heart. Free walls of the right and left ventricle were separated from the septum immediately lateral to their junction. The freed RV, septum and LV were then placed flat and were imaged by a gamma camera using a high sensitivity parallel collimator and an energy window for detection of 125 to 150 keV. The 1/10th control sample was imaged independently. Imaging was performed for 300 seconds, the image stored and the total number of counts recorded. A qualitative color image relating myocardial uptake the regions of myocardium to that area with greatest uptake was produced by the automated computer software. Each image was then reproduced after standardizing the number of recorded counts to the emission detected from the control sample and photographs taken of each image.

A quantitative analysis was also performed relating absolute counts in areas of myocardium to that obtained from the 1/10th control sample. The dose of TcPPT uptake by the myocardium was calculated as a percentage of the administered dose.

It had been identified in earlier animals that sampling myocardium had caused increased uptake of TcPPT in and around the area of sampling. Therefore an analysis of the uptake performed for the septum, which had not been traumatized by sampling, are only reported.

The photographs of gamma camera images were evaluated by two independent observers who were experienced in the analysis of images of the distribution of radioisotope in myocardium. They graded the images of the septum on a semi-quantitative scale of 0 to 4, 0 representing low uptake and 4 representing high uptake. A score was then awarded for the images of the whole heart.

Statistical analysis
Criteria for excluding hearts from evaluation included the presence of arrhythmias during preparation which potentially required DC cardioversion and failure of concurrent histological or radioisotope analysis. In fourteen animals the protocol was completed, providing four sham and ten active animals for analysis.

Data is presented as median values with 10th to 90th centiles. Non-parametric paired statistical tests were used to compare changes within a groups data and the Fisher’s exact test used to test the differences between groups. Correlation of paired data was tested with the Spearman’s method. Statistical significance was considered to have been achieved when p was less than 0.05.

Animals were treated in accordance with the guidelines of Animal Welfare described by the British Home Office. The experimental protocol was approved and licensed by the same body.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Hemodynamic status
The complete population of animals had stable ventilatory which was similar in the sham and BD groups, (Table 1). Sham animals remained hemodynamically stable from baseline onwards. The median systemic arterial pressure (SAP) at baseline was 50 mm Hg (10% to 90%, 41 to 56 mm Hg), the pulmonary arterial pressure (PAP) was 11 mm Hg (10% to 90%, 10 to 18 mm Hg) and the cardiac index was 3.1 L · min-1 · cm-2 (10% to 90%, 2.5 to 4.8). Only the heart rate increased from a median of 90 beat per minute (BPM), (10% to 90%, 70 to 114) to 114 BPM (10% to 90%, 100 to 134) in the terminal hour, p was less than 0.05.


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  		Table 1. Ventilatory Characteristics of Animal Groupsa

 
Hemodynamic characteristics of BD animals were statistically similar to those of sham animals at baseline. In subsequent hours animals showed marked individual variation. Some exhibited signs of autonomic hyperactivity whilst others exhibited early signs of autonomic extinction. An example of the former was an increase in the heart rate to 243 BPM, the mean SAP and PAP to 183 and 32 mm Hg respectively, and the CI to 10.2 L · min-1 · cm-2 directly related to the induction of intracranial hypertension preceding brain death. An example of early autonomic extinction was an absence of hypertension but a decrease in SAP to below baseline values between 10 and 30 minutes after induction of intracranial hypertension.

Following brain death four animals experienced premature cardiac arrest. In three it was preceded by cardiac indices below 2.0 L · min-1 · cm-2 and in the fourth it was preceded by a cardiac index of 3.5 L · min-1 · cm-2. In the latter marked ST elevation was recorded in lead II of the ECG and subendocardial hemorrhages were noted in the left ventricle after explantation. (NB Hemodynamic instability had been noted and TcPPT administered early, in practice this occurred approximately 1 hour before arrest occurred in these animals).

Creatine kinase (MB) subfraction release
The concentration of total CK rose in both sham and BD animals from baseline to the 6th hour, p less than 0.05, (Table 2). Only the change in CKMB values of BD animals from baseline to the latest sample was significant, p less than 0.01. Sham and BD groups did not differ at any time point.


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  		Table 2. Serum Concentration of Creatine Kinase and the MB Isoenzymea

 
Histochemistry
Sham hearts contained minimal histochemical evidence of injury at baseline and at subsequent time points. A maximum histological grade of 3 for ATPase disruption was recorded in 2, but SDH and MAO activity scores were 0, and thus total scores remained low (Table 3 and Fig 1).


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  		Table 3. Qualitative Imaging and Histochemical Analyses Grades, Survival of 6-Hour Experiment, and Terminal Cardiac Indexa

 


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  		Fig 1. Total histochemical grading of myocardium at baseline and the peak total value of severity after induction of brain death. The change in the BD group was significant p < 0.05. (Score 0 is equivalent to no myocyte injury with increasing severity to a grade of 12. Open points represent animals surviving the full procedure and closed points represent those that died prematurely.)

 
BD myocardium was similar to sham myocardium at baseline. Two patterns of change followed. The first was observed in 4 hearts in which no significant injury was identified by any test and the maximum total scores remained between 0 and 2 (Fig 1). In the remaining 6 hearts deterioration was noted early after brain death, grades 2 to 4 being recorded in each of the tests. The highest recorded total grades for each animal were between 4 and 11. Change of the values of the whole BD group were significant for the MAO, SDH and total values, p less than 0.05 for each. The degree of injury measured by these tests was significantly different from sham animals, {chi}2 p less than 0.05.

Three of the 4 episodes of cardiac dysfunction, as described above, affected the group of 6 hearts with marked histochemical injury. A sensitivity and specificity for peak total scores of values 4 and above predicting cardiac dysfunction was 75% and 33.3%. The positive and negative predictive capacity was 42.8% and 66.6% respectively.

Imaging myocardial uptake of TcPPT
Qualitative
Correlation between the scores awarded by the two observers was high, r = 0.86, p less than 0.0001, thus the average of their observations are reported in Table 3. The septa of sham hearts was graded 1.5 and below. Of the BD hearts the septum was graded 1.5 or less in six, and in 4 were graded from 2.5 to 4. Three of latter demonstrated cardiac dysfunction.

Quantitative
Uptake of TcPPT in septa correlated well with the total cardiac uptake and that of the left ventricle, r = 0.95 and r = 0.85, p less than 0.001 respectively. Median uptake by the sham septal regions was 0.0275% (0.002 to 0.061%) and by the BD group was 0.079% (0.042 to 0.492%) (Fig 2). Nine BD septa had greater uptake than the sham 90th centile value. In order to facilitate further analysis a value of twice the 90th centile values of shams was chosen and used as a cut off value, ie 0.122%. Thus six BD septa had uptake greater than this value (Fig 3).



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  		Fig 2. Graph showing the quantitative assessment of uptake of TcPPT by regions of the heart, calculated as a percentage of the total administered dose. (RV = right ventricle, LV = left ventricle. Solid bars represent 25th to 75th centiles and the error bars represent 10th to 90th centile).

 


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  		Fig 3. Graph showing values of quantitative assessment of the uptake of TcPPT by the septum with individual values plotted along side. (Solid bars represent 25th to 75th centiles and the error bars represent 10th to 90th centile. Open points represent animals surviving the full procedure and closed points those that died prematurely.)

 
Comparison of TcPPT uptake with histological parameters of injury
The correlation between TcPPT uptake determined by qualitative or quantitative imaging and injury quantified by histochemistry was determined for the population. Qualitative imaging correlated poorly with both quantitative imaging, r = -0.22, p equal to 0.34 and histochemical grades, r = -0.44, p equal to 0.27. Quantitative imaging of the septum correlated moderately well the total histochemical grade, r = 0.63 p equal to 0.02. Furthermore of those hearts with a histological grade of 4, a level of change considered to suggest significant injury, there was a significant relationship to TcPPT septal uptake greater than 0.122%, {chi}2 p equal to 0.008

Quantitative imaging of septal TcPPT uptake greater than 0.122% correctly identified 5 out of 6 BD hearts with significant histological injury, failing to identify one and incorrectly identifying another. The sensitivities and specificities of TcPPT uptake indicating myocardial injury was 83.3% and 75%, and positive and negative predictive values were 83.3% and 75%.

Additional data from excluded animals
The experimental methods of brain death induction were developed during the undertaking of this project. After techniques of induction of intracranial hypertension had been established, 21 animals were studied, but in the first 3 animals one of which was a sham, histological methods were evaluated only. In the sham septum TcPPT uptake was 0.042%. In a fourth animal, the quantitative imaging value was similar to sham animals, 0.031%, but histochemical data was absent. Evaluation of myocardial injury by quantitative birifringence, another method of assessment of myocardial injury utilized in the project, indicated the absence of myocyte injury. In fifth and sixth animals, both BD animals (L and S) terminal histochemical grades were 0 in each, but computer imaging data had been erased in error. Evaluation of isotope uptake by another method utilized in this project but not reported herein, recorded uptake of 0.0038 %/g and 0.0023%/g in septal tissue respectively and compared to the range of values in sham septa was 0.00044%/g - 0.0046%/g.

One sham animal (M) had, by intention, no myocardial samples obtained in order to provide an evaluation of the gamma camera imaging technique, in particular, the value of qualitative imaging, see the discussion. Quantitative assessment of uptake in the septum was 0.022%.


   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Patterns of myocyte injury in the hearts of patients suffering brain death are not uniform but vary in severity. The severity is related to the mechanism of injury leading to the occurrence of brain death. Brain death arising from a raised intracranial pressure, as for example following an acute intracranial hemorrhage, often causes a marked secondary autonomic response, evident as marked systemic and pulmonary hypertension, the Cushing effect [5]. This causes the tertiary effect of myocyte ischemia and injury [13, 14]. Mechanisms of brain death in which intracranial hypertension is not a principle feature of insult, eg acute and severe head trauma causing extensive parenchymal disruption may not be accompanied by the autonomic response and thus myocardial injury.

Hearts that are harvested for transplantation are obtained from cadavers that have suffered brain death and have received essential respiratory and possibly some cardiovascular support to maintain cardiac function. Evaluation of the suitability of a heart for transplantation involves a clinical assessment of cardiovascular stability of the cadaver [15]. Those cadavers which have been found to have a suitable evaluation are considered to have suffered a minimum of myocyte injury and likely to offer a reasonable prospect of good function in a recipient after transplantation. Clinical methods however, provide only an indirect and possibly inaccurate assessment of myocardial injury.

It is known that the degree of myocyte injury as assessed by histological criteria is not uniformly related to the cardiovascular status of the donor. In groups of transplanted hearts, as many as one third have suffered significant myocyte injury at the time of harvesting, a factor which may detrimentally affect both the short and long term prognosis of recipients [2, 3]. In a similar but opposite situation cadavers rejected from cardiac donation are a non-uniform group, many of which may not have received adequate resuscitation to identify their true potential for transplantation [15]. Thus the mechanism of brain death has been demonstrated to be related to the prognosis of recipients following transplantation, with hearts exposed to a significant Cushing reflex faring worst [7].

We tested the hypothesis that TcPPT would target injured myocytes and its uptake could be used as a direct quantification of myocyte injury induced by brain death. The model that was used was designed to allow a reproduction of the variable patterns of autonomic response to brain death that may be evident clinically and thus inducing varying degrees of myocardial injury. The results have demonstrated two important features regarding the use of the radioisotope infarct marker TcPPT. Firstly, they have demonstrated that in the situation of this model TcPPT could be avidly taken up by myocardium, sufficient to allow evaluation of its uptake, one hour after administration. Secondly, the results showed that there was greater uptake of TcPPT by some of the hearts subjected to the autonomic response of brain death and these hearts had suffered also greater myocyte injury.

There was a discrepancy between the results of quantitative and qualitative imaging. We believe this has arisen from the use of computer programming which automatically constructs color images with grades in color contrast relative to spots of greatest uptake. Thus images of hearts with a low but a uniform uptake over the heart may appear "hotter" on images than hearts with higher average uptake but with additional concentration of isotope at some sites. An attempt was made to overcome this anticipated error by relating the image to the standard. The quantitative data is naturally not influenced by this factor and thus prevents these discrepancies arising.

TcPPT is an infarct marker used in clinical practice to detect and quantify the size of an acute myocardial infarction, and has been shown to have clinical sensitivity and specificity in excess of 90% [16]. TcPPT binds to intracellular calcium targeting the areas of high calcium concentration in areas which have suffered myocyte necrosis and reversible myocyte ischemia. We have therefore deduced that our finding of preferential labeling by TcPPT of some hearts subjected to brain death indicates that these hearts have experienced a greater ischemic insult than sham hearts. This suggestion has been supported by the relationship of TcPPT uptake to the histological evidence of injury.

In an attempt to consider a role for a marker of myocyte injury in cardiac transplantation it may be perceived that such a tool has a significant positive potential but that there may be a significant negative element to its use. The latter may be perceived as it may be considered that a delineation of hearts additional to the present methods of evaluation for transplantation would diminish the donor pool. The contrary and positive situation we speculate may prove true. That is this test may be used to identify hearts considered to be unsuitable for transplantation following clinical assessment but which have suffered minimal myocyte injury. Some of these hearts may be salvageable by improved methods of resuscitation [17].

The utility of the infarct marker TcPPT has not been extensively investigated in the situation of cardiac transplantation. However in experimental studies McGregor demonstrated that rat hearts protected by St. Thomas’s Cardioplegia had reduced uptake of TcPPT compared with those unprotected [18]. In a similar model McGregor found that hearts transplanted to non-isogeneic animals that were not immunosuppressed experienced rejection that was detectable by uptake of TcPPT [19]. These results have not transferred to the clinical situation.

In summary we have used a model of brain death in which a range of myocardial injury has been induced similar to that described after clinical brain death. There appeared to be preferential uptake of TcPPT uptake by myocardium injured during brain death. We conclude that the utility of TcPPT as a marker of injury in potential donor hearts merits further investigation by evaluation. Consideration within these studies should be given to associated evaluation of myocardial function by echocardiography.


   Acknowledgments
 
We are grateful to the British Heart Foundation and the Killingbeck Childrens Heart Fund for the support given to this study.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Hosenpud J.D., Novick R.J., Bennett L.E., et al. The Registry of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant 1996;15:655-674.[Medline]
  2. Darracott-Cankovic S. Assessment of myocardial preservation during heart and heart-lung transplantation. Transplant Rev 1992;6:102-114.
  3. Darracott-Cankovic S., Stovin P.G.I., Wheeldon D., Wallwork J., Wells F., English T.A.H. Effect of donor heart damage on survival after transplantation. Eur J Cardiothorac Surg 1989;3:525-532.[Abstract]
  4. Cushing H. Concerning a definite regulatory mechanism of the vasomotor centre which controls blood pressure during cerebral compression. Johns Hopkins Hosp Bull 1901;126:290-292.
  5. Cooper D.K.C., Novitzky D., Wicomb W.N. The pathophysiological effects of brain death on potential donor organs, with particular reference to the heart. Ann R Coll Surg Engl 1989;71:261-266.[Medline]
  6. Connor R.C.R. Fuchsinophilic degeneration of myocardium in patients with intracranial lesions. Br Heart J 1970;32:81-84.[Free Full Text]
  7. Busson M., N’Doye P., Benoit G., et al. Donor factors influencing organ transplant prognosis. Transplant Proc 1995;27:1662-1664.[Medline]
  8. Parkey R.W., Bonte F.J., Meyer S.L., et al. A new method for radionuclide imaging of acute myocardial infarction in humans. Circulation 1974;50:540-546.[Abstract/Free Full Text]
  9. Satur C.M.R., Martin W., Darracott-Cankovic S., Morrison J., Wheatley D.J. An experimental method to induce variable patterns of brain death and myocardial injury. Transplant Proc 1998;30:211-213.[Medline]
  10. Chayen J, Bitensky L. Enzyme histochemistry. In: Chayen J, Bitensky L, eds. Practical histochemistry, 2nd ed. Chichester, UK: John Wiley and Sons, 1991:169–70, 219–39.
  11. Braimbridge M.V., Cankovic-Darracott S. Quantitative polarization microscopy and cytochemistry in assessing myocardial function. In: Pattison J.R., Bitensky, Chayen J., eds. Quantitative cytochemistry and its applications. New York: Academic Press, 1979:221-230.
  12. Darracott-Cankovic S., Bitensky L., Chayen J. Histochemistry of monoamine oxidase activity. Cell Biochem Funct 1986;4:109-110.[Medline]
  13. Simons M., Downing S.E. Coronary vasoconstriction and catecholamine cardiomyopathy. Am Heart J 1985;109:297-304.[Medline]
  14. Kolin A., Norris J.W. Myocardial damage from acute cerebral lesions. Stroke 1984;15:990-993.[Abstract/Free Full Text]
  15. Ghosh S., Bethune D.W., Hardy I., Kneeshaw J., Latimer D., Oduro A. Management of donors for heart and heart-lung transplantation. Anaesthesia 1990;45:672-675.[Medline]
  16. Berman D.S., Amsterdam E.A., Hines H.H., et al. New approach to interpretation of technetium-99m pyrophosphate scintigraphy in detection of acute myocardial infarction. Am J Cardiol 1977;39:341-354.[Medline]
  17. Iwai A., Sakano T., Uenishi M., Sugimoto H., Yoshioka T., Sugimoto T. Effects of vasopressin and catecholamines on the maintenance of circulatory stability in brain-dead patients. Transplantation 1989;48:613-617.[Medline]
  18. McGregor C.G.A., Hannan J., Smith A.F., Muir A.L., Wheatley D.J. A study of cold cardioplegic myocardial protection in rats. Cardiovasc Res 1983;17:70-74.[Medline]
  19. McGregor C.G.A., Hatz R., Aziz S., Billingham M.B., McDougall I.R. Technetium-99m pyrophosphate in diagnosis of acute cardiac rejection in the rat with effect of cyclosporine. J Nucl Med 1984;25:870-873.[Abstract/Free Full Text]
Accepted for publication May 26, 1999.





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