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Ann Thorac Surg 1995;60:1729-1734
© 1995 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Myocardial Effects of Experimental Acute Brain Death: Evaluation by Hemodynamic and Biological Studies

Georges Pinelli, MD, Paul-Michel Mertes, MD, PhD, Jean-Pierre Carteaux, MD, Yves Jaboin, Jean-Marie Escanye, PhD, François Brunotte, MD, Jean-Pierre Villemot, MD

Service de Chirurgie Cardiaque et Transplantations Cardio-thoraciques, Centre Hospitalo-Universitaire de Nancy-Brabois, and Laboratoires de Chirurgie Expérimentale and de Biophysique, Faculté de Médecine de Nancy, Vandoeuvre les Nancy, France

Accepted for publication July 29, 1995.


   Abstract
Top
 Footnotes
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. Because of problems concerning the functional quality of heart transplants, more and more interest has been focused on the physiologic changes occurring during brain death, one of the major possible contributing factors to the myocardial alterations.

Methods. The aim of this study was to describe the link between acute experimental brain death and myocardial metabolism. This was achieved by in vivo 3-hour hemodynamic and biological (myocardial lactate production) studies and then in vitro 6-hour phosphorus-31 nuclear magnetic resonance spectroscopy. Two groups of pigs were involved in the study: group I (n = 10) as control and group II (n = 10) as brain-dead animals.

Results. Within the first hour, we observed a strong increase in myocardial activity associated with the onset of myocardial lactate production, lasting 2 hours and corresponding to a myocardial anaerobic metabolism period. Despite the apparent normalization before excision of the hearts, phosphorus-31 nuclear magnetic resonance spectroscopy revealed a significant decrease in adenosine triphosphate levels in group II when compared with group I.

Conclusions. We conclude that, in our study, acute experimental brain death is associated with an early and transient period of myocardial anaerobic metabolism and adenosine triphosphate consumption. These myocardial consequences of brain death could partially explain some observations of heart graft dysfunction.


   Introduction
Top
 Footnotes
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Because of problems regarding the unexplained dysfunction of potential heart grafts before and after transplantation, more and more interest has been focused on the physiologic changes that may occur during brain death. Myocardial preservation (cardioplegia, cold storage) is thought to play a role in graft quality [1–4]. Many studies have been done concerning the hemodynamic [5, 6], hormonal [6, 7], metabolic [8], and histologic [9] changes occuring during brain death, one of the major possible contributing factors [10].

The aim of this study was to assess the link between acute experimental brain death in the pig and myocardial status using hemodynamic and biological studies including lactate determinations and phosphorus-31 nuclear magnetic resonance spectroscopic examination (high-energy phosphate compounds and intracellular pH determination).


   Material and Methods
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
All animals in this study received humane care in compliance with the ``Principles of Laboratory Animal Care'' formulated by the National Society for Medical Research and the ``Guide for the Care and Use of Laboratory Animals'' prepared by the National Institutes of Health (NIH publication 85-23, revised 1985).

Two groups of 10 common pigs (mean weight, 25 kg) were involved in the study: group I as the control group and group II as the brain-dead group. Both groups were submitted to the same protocol, with the exception of brain death in group II. They were premedicated with ketamine (20 mg/kg); anesthesia was induced and prolonged with 5 mg/kg (bolus) and 2 mg•kg-1•h-1 of thiopentone sodium administered intravenously. Mechanical ventilation was adapted to maintain blood gases within the normal range.

Experimental Brain Death
Experimental brain death in group II (n = 10) was induced by applying acute intracranial hypertension with an inflated Foley catheter balloon introduced into the subdural space. Brain death was confirmed by complete disappearance of electroencephalographic activity in less than 1 minute.

Hemodynamic and Biological Studies
Hemodynamic and biological data were systematically recorded 15 minutes before brain death induction as basal values, at the time of the subdural balloon inflation, and for the next 3 hours in group II. In group I, data were obtained at similar time intervals. Heart rate and mean arterial pressure were recorded continuously. After sternotomy, a catheter (Millar Mikro-Tip, Houston, TX) was introduced into the left ventricle via the apex to measure the left ventricular pressure and to determine its first derivative (dP/dtmax) as a contractility index. Serial blood samples were drawn to monitor lactate levels in arterial and coronary sinus blood. Myocardial lactate production was defined as a negative result of the arterio--coronary sinus difference.

Heart Excision and Preservation
After 3 hours of brain death in group II, corresponding to a control period in group I, hearts were excised for spectroscopic study. The cardioplegia as well as the excision and the hypothermic storage method were similar to those used for myocardial protection in clinical situations. The aortic cross was clamped. One liter of cold cardioplegic solution (St. Thomas' Hospital solution [Plegisol]; Abbot Laboratories, North Chicago, IL) at 4°C was infused into the aorta. The heart was excised and stored in a hermetic container with physiologic serum at 4°C. The container was placed in an isothermal box filled with crushed ice.

Phosphorus-31 Nuclear Magnetic Resonance
During the 6-hour cold preservation time, 31P nuclear magnetic resonance spectroscopy was used to evaluate changes in intracellular high-energy store. A Bruker Biospec/Medspec BMT 100 in-vivo spectrometer equipped with a horizontal 40-cm-bore-diameter 2.4-Tesla magnet was used for determinations of the spectra. The hearts remained in their containers during the measurements. A 5-cm-diameter double-turn-plate surface coil was placed in contact with the container's flat bottom wall. This allowed a hemispheric sensitive volume equal to about 10% of the measured heart volume. Measurements were performed on a sensitive volume without precise localization.

The coil was tuned to 100.18 MHz for protons to shim the static magnetic field and to 40.65 MHz for phosphorus signal recording. A signal was obtained from an average of 200 free induction decays after the CYCLOPS signals pulse four phases cycling sequence. A repetition time of 1 second was used. A pulse angle of 70 degrees was chosen to maximize the signal. Because of these fast acquisition rates, longitudinal relaxation times of phosphorus peaks were measured separately to correct signal intensity. Average values at 4°C were recorded as follows: inorganic phosphates (Pi), 5.2 seconds; phosphocreatine (PCr), 4.1 seconds; and beta-adenosine triphosphate (ß-ATP), 3.4 seconds. Spectra (Fig 1Go) were obtained using Fourier transformation after 14-Hz line broadening. Gross baseline distortions were first corrected by manual subtraction of a quadratic polynomial fit. Simultaneously, PCr peaks were shifted to the same frequency for automatic processing comprising a baseline of least square linear fit, peck windowing, integration, and tabular presentation of data for statistical processing. Rates for ß-ATP/S, Pi/S and PCr/S, where S is the total phosphorous pool, are presented in the Results section. Peak area errors were estimated to lie within a 7% range.



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  		Fig 1. . Spectra obtained during the 6-hour cold preservation time by in vitro 31P nuclear magnetic resonance spectroscopy. (ßATP = beta-adenosine triphosphate; PCr = phosphocreatine; Pi = inorganic phosphate.)

 
Intracellular pH was determined using the Dawson [11] formula at 4°C: pH = 6.88 + Log10 [({delta}-3.35)/(5.6-{delta})], in which {delta} represents the chemical shift between PCr and Pi. As the spectral width was 2,000 Hz and the memory size for each spectrum was of 1 K-word, errors affecting these values were estimated in the 0.15 pH unit range. Measurements were performed every 30 minutes after heart excision.

Statistical Analysis
Results are expressed as a mean ± standard deviation of the mean. The two groups were compared with the nonparametric Friedmann's (repeated data) and Mann-Whitney's tests. Significance was accepted for p values less than 0.05.


   Results
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Hemodynamic Data
Hemodynamic data are summarized in Table 1Go. In group II, after the induction of brain death, a significant increase in heart rate, mean arterial pressure, and dP/dtmax began in the first 5 minutes and returned to less than basal values within 60 minutes.


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  		Table 1. . Hemodynamic Changes During Induced Brain Deatha
 
Over the next 2 hours, mean arterial pressure was significantly reduced in brain-dead animals when compared with the control group. No significant differences were observed between the two groups in heart rate and dP/dtmax during this time.

Lactate Examinations
Arterial lactate levels remained stable in both groups during the entire study period (Fig 2Go), suggesting persistant normal aerobic condition in the whole body during brain death. Conversely, significant myocardial lactate production was observed in brain-dead animals (Fig 3Go), indicating the onset of functional myocardial ischemia. This period of myocardial anaerobic metabolism remained significant until 120 minutes after brain death induction. Normal myocardial lactate uptake was restored at 180 minutes. At the time of heart excision, normal myocardial lactate consumption was restored in group II.



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  		Fig 2. . Biological data: serum lactate levels. There is no lactate production by the whole body during the initial brain-death period, suggesting persistant aerobic condition.

 


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  		Fig 3. . Biological data: lactate level difference between arterial and coronary sinus blood (a-v). The onset of significant myocardial lactate production from 30 minutes until 120 minutes after brain death induction demonstrates the myocardial anaerobic metabolism during induced brain death. Myocardial metabolism was restored at 180 minutes.

 
Phosphorus-31 Nuclear Magnetic Resonance Results
The 31P nuclear magnetic resonance data were summarized in Figure 4Go. During the 6-hour cold preservation period, we observed a similar decrease in PCr/S levels and intracellular pH and a similar increase in Pi/S levels in both groups. During the same period, ß-ATP/S levels remained stable but were significantly lower in group II (brain death) than in group I (control).



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  		Fig 4. . Phosphorus-31 nuclear magnetic resonance spectroscopic results: rates for phosphocreatine/total phosphorus pool (PCr/S), inorganic phosphate/total phosphorus pool (Pi/S), beta adenosine triphosphate/total phosphorus pool (beta ATP/S), and intracellular pH (pHi) obtained during a 6-hour preservation time are presented. The only significant (p < 0.05) difference between the two groups is the bATP/S level, lower in the brain-dead group than in the group control.

 

   Comment
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
These results suggest that acute experimental brain death is associated with major, immediate, and transient hemodynamic changes and with the onset of a myocardial anaerobic metabolism period. Despite aerobic myocardial metabolism restoration before heart excision, adenosine triphosphate (ATP) level remains depressed in group II during the entire study period.

Our experimental brain death is simple and reliable and occurs suddenly. It was preferred to the vascular cervical or thoracic ligatures as they induce a delayed brain death. However, as shown by Shivalkar in dogs [12], severe histologic myocardial damage as necrosis occurred after acute intracranial pressure increase, but histologic myocardial damage appeared to be milder after a gradual intracranial pressure increase.

Hemodynamic changes during brain death are consistent with those reported previously by our group and others [4, 6, 13]. In our experimental study, they occurred suddenly and were short-lasting. The early brain death period was also characterized by the onset of functional myocardial ischemia as attested by myocardial lactate production, without affecting overall anaerobic metabolism. The lack of anaerobic metabolism in the whole body, as we describe in our study, somewhat diverges from the results of other experimental studies describing hormonal depletion as a major factor of heart graft dysfunction [7, 8] occurring during brain death. However, controversy still persists concerning this fact [14, 15]. After the initial functional myocardial ischemia, a progressive return to normal myocardial lactate consumption was observed 2 hours after brain death. In a previous experimental study [16], we demonstrated an upset in the regulatory mechanism of coronary blood flow resulting in an imbalance between myocardial oxygen requirement and oxygen delivery, which might be related to a sustained increase in myocardial interstitial neuropeptide Y concentrations [17, 18] with a direct vasoconstrictor effect [19, 20].

The occurrence of functional myocardial ischemia during brain death underlines the importance of myocardial energetic metabolism studies. Phosphorus-31 nuclear magnetic resonance spectroscopic examination allows noninvasive and repeated measurement of myocardial high-energy phosphate storage and intracellular pH [21, 22]. It is a relevant method for heart viability evaluation during hypothermic or normothermic ischemia [23–27].

Our results show, in both groups, a decrease in pH and PCr/S levels and an increase in Pi/S levels in relation to the cold ischemic preservation time [21, 28–30]. The ß-ATP/S levels were stable in both groups, but these were lower in group II than in group I.

Concerning ß-ATP/S stability, our results somewhat diverge from those reported by Forester and associates [25]. In this study, a regular ß-ATP decrease was noted. However, the cardioplegic solution was administered after heart excision. In our opinion, an initial warm ischemia, even short-lasting, might have led to increased ß-ATP consumption. On the contrary, in studies using protocols similar to ours [28, 31], stability of myocardial ATP level was described and a decrease occurred only after 6 hours of preservation.

However, these studies using 31P nuclear magnetic resonance spectroscopy have not included the effects of brain death, which, in our experiments, led to reduced myocardial ATP levels. This is confirmed by some experimental studies using biochemical evaluation of myocardial high-energy compounds. They showed a decrease in ATP level after warm myocardial ischemia and brain death [32, 33]. Moreover, 31P nuclear magnetic resonance evaluation of myocardial high-energy phosphate storage is more accurate than biochemical evaluation in myocardial biopsy specimens, which must be quickly frozen to prevent ATP consumption.

We noted similar PCr/S levels in both groups, an unexpected result in view of the disparity in ATP levels in the two groups. This may be explained by a shorter PCr reversion time versus ATP reversion time as described in other experiments [34–37]. In our study, hemodynamic and biological data suggest restored normal myocardial perfusion conditions before heart excision. This return to normal myocardial status might be sufficient to allow PCr recuperation, but not ATP rehabilitation.

As ATP is usually considered as a viability index [21, 30, 38], its measurement using 31P nuclear magnetic resonance can provide reliable indices for predicting postreperfusion ventricular contractility [28]. Moreover, this technique can also provide information concerning accumulation of Pi and intracellular acidification, which might also be useful in potential heart graft evaluation [29].

In these conditions, our results suggest that brain death could be a major cause of heart function impairment and so could partially explain the occurrence of some cases of heart failure in brain-dead patients and in human heart recipients. The apparent normalization of hemodynamic parameters and myocardial lactate consumption we observed does not preclude a latent myocardial dysfunction. This was confirmed in a previous study using a volemic expansion test [13]. In that report, the same protocol concerning brain death was used, resulting in the same hemodynamic consequences compared with the present study. In these conditions, the acute preload increase revealed an impaired myocardial contractility, confirmed by a decrease in dP/dtmax and cardiac output and by an increase in serum lactate levels.

In conclusion, our results are consistent with those reported by previous authors who suspected direct myocardial impairment resulting from cerebral lesions. They are also in accordance with those described during warm ischemia and reperfusion. Our study suggests that the effects of brain death on the myocardium include the onset of a transient anaerobic metabolism period with alterations in its high-energy compound, specifically in an ATP decrease. This could partially explain myocardial dysfunction after heart transplantation.


   Acknowledgments
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
We thank Mrs Jacqueline Zevnick for her assistance in translating and editing of the manuscript.

This work was in part supported by a grant from INSERM (CRE 015, France).


   Footnotes
Top
 Footnotes
Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Address reprint requests to Dr Pinelli, Service de Chirurgie Cardiaque et Transplantations Cardio-thoraciques, CHU Nancy-Brabois, Rue du Morvan, 54500 Vandoeuvre les Nancy, France.


   References
Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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