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Eur J Cardiothorac Surg 2005;28:576-580
© 2005 Elsevier Science NL

Original articles

31P MRS of heart grafts provides metabolic markers of early dysfunction

Thierry Caus a , b , * , Frank Kober a , Annick Mouly-Bandini b , Alberto Riberi b , Dominique R. Métras b , Patrick J. Cozzone a , Monique Bernard a

a Centre de Résonance Magnétique Biologique et Médicale (CRMBM), UMR CNRS 6612, Fac. Med., 27 Bd Jean Moulin, 13005 Marseille, France
b Service de Chirurgie Cardiaque, CHU Timone, 13005 Marseille, France

Received 1 June 2005; received in revised form 8 July 2005; accepted 13 July 2005.

* Corresponding author. Address: Service de Chirurgie Cardiaque, CHU Timone, 13005 Marseille, France. Tel.: +33 491 324471; fax: +33 491 256539. (Email: tcaus{at}ap-hm.fr).

Abstract

Objective: Early graft failure (EGF) is a life-threatening event still accounting for a significant percentage of early deaths after heart transplantation. We tested whether selected metabolic markers, including high-energy phosphate concentrations measured ex vivo in pre-transplant heart grafts by 31P magnetic resonance spectroscopy (MRS) are related with early post-transplant outcome. Methods: During a 3-year period, 26 heart grafts harvested in the vicinity of the transplantation centre were studied. Evaluation of transplantability was done conventionally. 31P MRS was performed ex vivo approximately 60min after aortic cross-clamp to quantify ATP, Pi and PCr concentration ratios. A MRS-score was defined as a combination of intracellular pH (pHi) and the PCr/Pi ratio. EGF was defined as the need to abnormally extend circulatory support or to use more than two inotropes before weaning the patient from CPB after transplantation. The grafts were attributed to three groups as follows: A1, transplanted with uneventful outcome (n=14); A2, transplanted with subsequent EGF (n=3) and B, not suitable for transplantation (n=9). Results: Significant differences between groups existed for the following metabolic markers: PCr/ATP (P=0.013), PCr/Pi (P=0.0004), pHi (P=0.0016) and MRS-score (P=0.0001). The sensitivity, specificity and positive likelihood ratio for EGF with a MRS-score≤1.95 were, respectively, 100%, 86% and 7. Conclusions: In the setting of this study, post-transplant outcome was related to the pre-transplant MRS-score of grafts evaluated ex vivo. This result might help to more securely use grafts from marginal donors.

Key Words: Heart transplantation • Graft failure • Phosphorus magnetic resonance spectroscopy

1. Introduction

Early graft failure (EGF) [1,2] is a dramatic complication of heart transplantation (HTx) that remains one of the primary causes of early deaths. When facing primitive myocardial dysfunction, organ damage during the transplant process is likely to be involved. The current quality assessment of heart grafts before harvesting is partly subjective or operator dependent. Therefore, detection of organ damage may be inadequate. Possible risks for organ damage include brain death, donor resuscitation, cardioplegia, graft harvesting, prolonged ischaemic time—particularly in case of aged donors—and reperfusion. The growing interest to use organs from marginal donors due to the current organ shortage has stimulated the need for objective metabolic markers of myocardial damage in the setting of heart transplantation.

Metabolic evaluation of the human heart graft has been performed in a few recent studies based on biological analyses from blood samples or from biopsies with different endpoints and limitations. Blood sample analyses in heart donors aimed at measuring the circulating amount of biological markers known to be released in the blood stream by the injured myocardium. As a recent example, high plasma levels of troponin T (cTnT) and of procalcitonin (PCT) measured in blood samples have been shown to be related to EGF suggesting that cTnT and PCT are reliable metabolic markers of myocardial damage resulting from brain death and resuscitation [3,4]. However, this measure performed in blood samples of donors can only assess the pre-harvesting status of the graft. Based on the energy charge theory [5], a recent study on human donor heart biopsies [6] showed no relationship of high-energy phosphate adenine nucleotides across transplantation with the post-transplant haemodynamic performance of the heart graft. That study, however, only evaluated adenine nucleotide compounds and had limitations associated with the biopsy procedure.

In a previous study, we demonstrated a strong correlation between the current clinical evaluation of heart grafts and some selected metabolic markers measured by 31P magnetic resonance spectroscopy (MRS) 1h after harvesting [7,8]. In this preliminary study, however, we did not address whether this result is related with post-transplant outcome. In the present study, we verified whether the occurrence of early heart graft failure is related to the values of selected markers of ischaemia determined by 31P-MRS analysis. Selected metabolic markers include the phosphocreatine (PCr)/ATP and the PCr/inorganic phosphate (Pi) concentration ratios, intracellular pH (pHi) as well as a MRS-score [7] combining pHi and PCr/Pi. For this purpose, a series of 26 human hearts harvested from multi-organ donors was submitted to a MRS protocol.

2. Materials and methods

This pilot study was conducted between January 2000 and December 2003 under approval by the local Ethics Committee for biomedical research. The result of the MRS study did not interfere with the decision to transplant the graft.

2.1 Graft allocation policy
Twenty-six heart grafts harvested from multi-organ donors in the greater Marseille district were recruited for this study. Grafts were harvested from heart-beating, brain-dead donors. Clinical evaluation of grafts was based on the usual criteria: age of donor, level of inotropes administered before harvesting, left-ventricular function (ejection and/or shortening fraction assessed by echocardiography) and clinical assessment by the harvesting surgeon [7]. As a result of our institutional policy that aims at increasing the pool of grafts available for transplantation, hearts harvested locally from marginal donors were also systematically checked for transplantation. Marginal donors were those failing to meet at least one of the traditional criteria for an optimal cardiac donor [9]. Hearts harvested from older donors (age above 55 years) or those presenting ventricular dysfunction (left ventricular dysfunction below 45%) detected by pre-harvesting echocardiography were not transplanted when inotropes or vasopressors had to be applied at high doses (above 5µg/kg per min). Management of donors was conventional with no attempt to resuscitate the heart before harvesting as opposed to currently proposed guidelines [9]. Right catheterisation for haemodynamic measurements was not used in routine, and adjustment of inotropes and fluid was empirically done such as to maintain the mean arterial pressure above 60mmHg.

2.2 Transplantation process
Regardless of their eligibility for transplantation, all hearts were conditioned identically. Celsior® solution was used for cardioplegia and as storage buffer. Once harvested, the grafts were placed into sterile bags sealed and introduced into plastic jars. Jars were placed in a cooling box filled with crushed ice. They were directly brought to the MRI–MRS facility situated within the hospital performing the transplantation. Transplantation was performed using the standard (n=10) or the bi-caval technique (n=7) according to the surgeon's preferences and skills. Reperfusion of the graft was pressure-controlled and conducted under total aortic clamp until the heart restarted beating, and until the blood pressures equalised up- and down-stream the aortic clamp. Pharmacological management of recipients started immediately after reperfusion and included Isoprenalin initiated at 5µg/kg per min and increased if needed, inhaled nitrous oxide and Adrenalin up to 5µg/kg per min whenever required. Following our regular protocol, a third inotrope/vasopressor was then administered according to the recipient's haemodynamic profile instead of increasing the doses of Adrenalin above 5µg/kg per min. The surgeon was kept blinded from the result of the MR study throughout the transplantation process. The immunosuppression regimen was based on a triple drug association including prednisone started immediately before transplantation.

2.3 MR protocol
The complete protocol has been previously detailed [7]. Briefly, MRS was performed using a commercially available 31P-1H surface coil in the magnet of a Siemens Vision Plus 1.5 T MR system (Siemens Medical Solutions, Erlangen, Germany). During the procedure, the heart was kept inside the ice container that was placed on the surface coil. The MR protocol included MRI for localisation purposes followed by a 31P one-pulse MRS sequence to obtain global spectra at 25.9MHz. The resonance amplitudes of Pi, PCr and {gamma}ATP were calculated using AMARES time domain fitting. ATP concentration was considered to be represented by the {gamma}ATP signal amplitude. pHi was calculated from the chemical shift difference between PCr and Pi. A MRS-score was defined combining pHi and PCr/Pi as follows: MRS-score=PCr/Pi+pHi–7. The total duration of the MR procedure (from graft arrival to departure from the MR facility) did not exceed 35min.

2.4 Group definition
As a function of the clinical evaluation and transplantation outcome, the grafts were retrospectively assigned to three groups: A1, transplanted grafts with uneventful outcome (n=14); A2, transplanted grafts with early graft dysfunction (n=3) and B, grafts not suitable for transplantation (n=9). The primary endpoint of this study was occurrence of EGF defined by at least one of the following events: (i) occurrence of post-operative death (30 days mortality) due to myocardial failure; (ii) need to prolong the cardiopulmonary bypass (CPB) time over half the graft's ischaemic time or to add a third inotrope/vasopressor to our current medication protocol or to insert an intra-aortic balloon pump, ECMO or any mechanical assistance device; (iii) myocardial failure revealed by low cardiac output with normal pulmonary resistances assessed by post-operative echocardiography.

2.5 Statistics
Statistical analyses were performed using SPSS statistical programs (SPSS, Inc., Chicago, IL). All values are expressed as mean±standard deviation (SD). Differences between groups were evaluated using a non-parametric Kruskal–Wallis analysis test and were considered significant when P<0.05. Considering the observed prevalence of early graft failure in the transplant recipients, the best cutoff values were calculated for each considered metabolic marker by using ROC curves to optimise sensitivity and specificity expressed with their respective 95% confidence interval. We also characterised tests by calculating positive and negative likelihood ratio (respectively, +LR and –LR) as well as positive and negative predictive value (respectively, +PV and –PV).

3. Results

3.1 Clinical results
Available demographic data on the donors are presented in Table 1 . Ischaemic time before 31P-MRS was 63±21, 68±8 and 69±18min in groups A1, A2 and B, respectively (P=0.74). The prevalence of early graft failure was 3/17 (17.6%). Clinical outcome was favourable for every patient receiving grafts from group A1 with no early death post-transplantation and easy weaning from respiratory support and a mean stay in the intensive care unit of 10±2 days (in accordance with our institutional average of length of stay in ICU). Two patients receiving grafts from group A2 died during early course following transplantation. One died from sudden cardiac arrest at the third postoperative day, the other from severe respiratory infection favoured by prolonged respiratory assistance. Both patients presented postoperative low cardiac output with ventricular dysfunction. The third graft from group A2 recovered ad integrum from early failure allowing for progressive successful weaning of the recipient from pharmacological support. No graft from group A2 was transplanted under the condition of a BSA mismatch with the recipient, in a situation of elevated pulmonary resistances or in patients under pharmacological or mechanical circulatory support.


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  		Table 1. Donor characteristics
 
3.2 MRS results
The MRS data for each group are shown in Table 2 . A scatter plot representation of the distribution of the MRS-score within each group is given in Fig. 1 . Evaluation of predictive test for EGF after reperfusion based on each studied metabolic marker considering the best cutoff value is given in Table 3 . The MRS-score showed a higher sensitivity with an increased positive likelihood ratio and positive predictive value than the directly measured values.


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  		Table 2. MRS findings for each studied group. Values are expressed as mean±SD
 


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  		Fig. 1. Distribution (scatter plot) of the MRS-score between groups A1, A2 and B. For each group the mean value and mean±SD are graphically represented. The dashed gray line represents the cutoff value of the MRS-score (1.95). All but two grafts from group A1 are above the cutoff value, whereas all grafts from groups A2 and B are below the cutoff value.

 

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  		Table 3. Sensitivity, specificity, positive and negative likelihood ratio, positive and negative predictive values for predictive tests of EGF after reperfusion based on the optimised cutoff values for PCr/ATP, PCr/Pi, pHi and MRS-score
 
4. Discussion

Metabolic investigation of the heart graft may be an important issue for expanding the use of marginal donors. In a previous paper, we found that metabolic markers determined by 31P-MRS were objective criteria for the decision to accept or refuse heart grafts [7]. The results presented here clearly show lower values of PCr/ATP, PCr/Pi, pHi and MRS-score in grafts presenting early failure compared with well performing hearts. On the other hand, non-transplanted grafts had significantly lower pHi and presented lower metabolic ratios and MRS-scores compared with well-performing transplanted hearts. This finding suggests that these hearts may have suffered from pre-transplant myocardial injury and therefore confirms the clinical assessment. Moreover, transplanted hearts presenting EGF at reperfusion had a pHi within the range of non-transplanted hearts and an only slightly higher MRS-score. In these cases, however, the conventional clinical evaluation failed to detect pre-transplant myocardial injury. The MRS-score proposed here may be considered as a potential additional criterion in a metabolic approach aiming at securely recruiting grafts from marginal donors. Based on the observed prevalence of EGF in the current study, we found the positive and negative predictive value of the diagnostic test (MRS-score≤1.95) to be 60 and 100%, respectively. This suggests that EGF is unlikely to happen for a MRS-score above 1.95 in the conditions of our study (absence of high pulmonary resistances or donor/recipient mismatch, time between aortic clamping and MR study about 1h). Therefore, in case of marginal donors, higher MRS-scores could help in taking the decision to transplant the graft into selected recipients. On the other hand, MRS metabolic markers might not reflect irreversible injury as opposed to metabolic markers, which reflect cellular lyses. For this reason and because of the rather low positive predictive value, a lower MRS-score would not be sufficient to take the decision to refuse the graft.

High-energy phosphates (HEP) are well known to vary with ischaemia and reflow but the relationship between HEP and myocardial function is still a matter of controversy. Van Dobbenburgh et al. [10] have shown a relation between the metabolic condition of the graft assessed during cold storage and the functional recovery one week after transplantation evaluated by right catheterisation during the first biopsy procedure. These authors studied functional recovery one week after transplantation while our study focused on early graft failure occurring immediately after reperfusion. An early assessment of EGF is more appropriate when the direct effects of the ischaemia-reperfusion sequence on myocardial contractility are to be studied. In the study by van Dobbenburgh et al., metabolic ratios were calculated at varying ischaemic durations using a correction algorithm. In our study, the time between aortic clamping and MR studies was maintained within a very close range by limiting the populations to locally harvested grafts. Time-related effects on the results were hereby avoided.

In a more recent study, Stoica et al. [6] found no correlation between HEP adenine nucleotides and allograft function in the post-operative period. Adenine nucleotides were determined by chemiluminescence performed on repeated biopsies across the transplant process, but not during storage. In our study, MRS was used as a non-invasive metabolic investigation tool that permitted measurements during organ storage. We also measured PCr and intracellular pH that are both well-known markers of ischaemia. Given these differences in methodology, our results are not in contradiction with those reported by Stoica et al. Phosphocreatine and pHi are shown here to be important markers for graft quality assessment. Both are already well-established markers of ischaemia. We observed significant differences in phosphorus metabolite ratios and pHi after 1h of cold storage. Particularly during this time, the metabolites are influenced by a variety of events beginning at brain death [7]. These events modulate the status of the myocardium leading to failure or complete recovery at reperfusion.

Biological markers like cTnT or PCT measured in blood samples from heart donors have already been shown to indicate propensity for early graft failure. However, it is evident that no post-harvesting myocardial injuries [3,4] can be detected when donor blood samples are used. Damaging events related to brain death, for instance, may be revealed only during the ischaemic period corresponding to the cold storage time [11]. Measurement of these markers in the cardioplegic liquid would therefore be of particular interest. In fact, a preliminary study [12] suggests that troponin I measured after transport in the cardioplegic liquid may be an index of early graft failure.

The relation between an increased ischaemic time and occurrence of EGF is currently unclear in clinical settings [13,14]. However, since EGF may be initiated by an extended period of ischaemia, this study was limited to regional donors, thereby keeping the transport time short. The total ischaemic time from harvest to transplantation always remained shorter than 3h and never even attained the ischaemic time usually observed with non-regionally harvested grafts. Additional risks for recipients induced by the MRS exam were therefore excluded, but this also implies that for heart grafts harvested at long distance, a shorter MRS protocol would be necessary. At this time, MRS evaluation would probably be most useful for grafts harvested from marginal donors. And in practice, long distance grafts from marginal donors are only rarely considered for heart transplantation.

Although P-31 MRS is not applied in routine in clinics several studies have shown its potential to detect alterations in different cardiovascular pathologies [15–17]. Clinical relevance of 31P-MRS for heart graft evaluation is, however, not proven at this time. To our knowledge, only two studies have focused on the potential interest of 31P-MRS performed on isolated hearts before transplantation in human recipients [7,10]. The results of both studies have led to the conclusion that 31P-MR spectra of heart grafts might be related to the current transplantability assessment before harvesting and to the haemodynamic performance of the heart one-week post-transplant, respectively. In the setting of the institutional report presented here, we show that transplant outcome is related to the pre-transplant MRS-score. If validated by a larger multi-institutional study including a greater number of grafts, heart evaluation by 31P-MRS before transplantation could be considered as clinically relevant and promote the application of magnetic resonance techniques for metabolic evaluation of other solid organs before transplantation.

4.1 Limitation of the study
Making a potential donor non-eligible for heart transplantation and therefore assigning the corresponding heart graft in group B was a result of our institutional policy. A different institutional policy might have resulted in transplanting some of these hearts, which would possibly have induced changes in the results of our study. Comparing our institutional policy with that of other centres shows, however, a close agreement since all grafts from group B were also refused for transplantation when proposed to other institutions. The study has been initiated before the adoption of cTnT measurements on donor blood samples as a routine test for evaluation of human graft in our centre. Therefore, we could not correlate MR data with this predictive parameter of early graft failure.

5. Conclusion

The current shortage of heart donors requires an expansion of the pool of available organs by accepting grafts from marginal donors. In this context, objective characterisation of heart grafts is mandatory. This study is a step forward in evaluating ex vivo 31P-MRS as an objective method to assess the quality of human heart grafts. Nevertheless, the exam needs to be definitely validated by a larger multi-institutional study including a greater number of grafts. Keeping in mind the rapidly growing availability of MR facilities, 31P-MRS analysis of heart graft might in future contribute to better screen hearts from marginal donors.

Acknowledgments

Programme Hospitalier de Recherche Clinique 2001 (Assistance Publique-Hôpitaux de Marseille). Centre National de la Recherche Scientifique (UMR 6612). We greatfully acknowledge Drs Sylviane Confort-Gouny, Marguerite Izquierdo, Yann Le Fur and Jean-Philippe Ranjéva for technical support.

References

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