Ann Thorac Surg 1996;61:679-683
© 1996 The Society of Thoracic Surgeons
Original Article: Cardiovascular
Comparisons of Methods of Myocardial Hypothermia for Cardiac Transplantation
Pat O. Daily, MD,
Robert M. Adamson, MD,
Barbara H. Jones, RN,
Walter P. Dembitsky, MD,
Ricardo J. Moreno-Cabral, MD
Sharp Memorial Hospital, San Diego, California
Accepted for publication October 16, 1995.
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Abstract
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Background. Myocardial hypothermia of less than 10°C is an essential component of preservation of donor hearts before implantation. Here we report temperature changes and comparison of methods for maintenance of myocardial hypothermia during implantation.
Methods. Twenty patients were prospectively randomized into two equal groups. In one cohort myocardial hypothermia was maintained by the ``Stanford method'' of continuous lavage of the pericardium and left atrium with refrigerated saline solution. In the other a cooling jacket was used without saline lavage. Temperatures at multiple sites were measured at 30-second intervals from initiation of cardiac suturing until aortic cross-clamp removal. Comparisons were made between groups at each temperature site.
Results. The cooling jacket group temperatures were significantly lower at the left ventricular epicardium and endocardium than those of the Stanford method group.
Conclusions. During cardiac implantation maintenance of myocardial hypothermia with a cooling jacket resulted in significantly deeper and more consistent hypothermia of the left ventricle than pericardial and left atrial lavage with refrigerated saline solution. Blood loss from aspirated saline lavage and perfusate dilution by the saline solution were eliminated.
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Introduction
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Maintenance of profound myocardial hypothermia (4°C) after harvesting of the donor heart is the primary modality for continued myocardial preservation until implantation. Persistent maintenance of profound hypothermia during cardiac implantation is desirable to maximize myocardial protection. Perhaps the most common method of maintaining myocardial hypothermia during implantation is the ``Stanford method'' (SM), which involves myocardial surface cooling with continuous irrigation of hypothermic saline solution at 4°C [1] and, more recently, continuous instillation of hypothermic saline solution through the left atrium after the left atrial suture line has been completed [2]. However, the efficacy of maintenance of myocardial hypothermia with this method is not clear.
Previous studies of myocardial hypothermia obtained by the SM [1] for valve replacement demonstrated that the surface cooling technique was suboptimal [3] and that the use of a cooling jacket (CJ) resulted in more consistent and deeper myocardial hypothermia [4]. Other studies have addressed myocardial heat transfer and optimization of myocardial hypothermia [5, 6]. Also, a CJ has been shown to be superior to multidose cardioplegia for myocardial temperature control in patients undergoing coronary artery bypass grafting [7]. Consequently, this study was undertaken to compare myocardial temperatures at multiple sites during implantation of the donor organ with the SM with those obtained with a CJ but without intracardiac saline lavage.
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Patients and Methods
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Sharp Memorial Hospital Investigative Review Committee approved the study protocol and informed patient consent was obtained. Over an 18-month period, patients undergoing cardiac transplantation were randomized prospectively into two equal groups. The mean age was 54 ± 9 years (range, 65 to 30 years). There were 2 women and 18 men. In 10 patients (SM group) myocardial hypothermia during implantation was maintained by the SM wherein continuous irrigation of the pericardial cavity was performed with refrigerated saline solution. Additionally, saline solution at the same temperature was continuously instilled through the left atrium. In another group of 10 patients (CJ group), a myocardial CJ (Medtronic-Daily; Medtronic Cardiopulmonary, Anaheim, CA) was positioned in the pericardial cavity after removal of the recipient heart. The donor heart was placed in this CJ, and all suture lines were completed before removal of the jacket.
Surgical Methods
The surgical approach was the same in both groups of patients. The donor heart was procured after aortic cross-clamping and instillation of 1 L of hypothermic cardioplegia, the Stanford solution [8]. Before the heart was placed in an ice chest for transport, it was immersed in a bag of saline solution, which was subsequently placed in two additional bags of iced saline solution. Temperatures were not measured during transportation of the donor heart.
After median sternotomy in the recipient, bicaval cannulation was performed directly with Pacifico (DPL Co, Ann Arbor, MI) cannulas. The ascending aorta was cannulated and cardiopulmonary bypass was instituted. On arrival of the donor heart, the aortic cross-clamp was applied and cardiectomy performed in the recipient.
In the SM group intravenous tubing was sutured to the pericardium and continuous instillation of refrigerated saline solution was started. With completion of the left atrial suture line, more saline solution was lavaged through the left atrium. The suture lines of both groups were performed in the following sequence: left atrial, right atrial, pulmonary artery, and aortic. In the CJ group, after excision of the recipient heart, a sump tube was placed through the right superior pulmonary vein into the left atrium. This sump tube was connected to the cardiotomy system with continuous aspiration for removal of blood entering the left atrium via the pulmonary veins. The sump was removed after completion of the aortic suture line. The cooling jacket was placed in the pericardial cavity before positioning the donor heart for suturing, precluding contact of the donor myocardium with any warm recipient tissue. The donor heart was placed inside the cooling jacket and the left atrial suture line was started (Fig 1
). The pulmonary artery suture line is seen in Figure 2. (Suture lines were performed as described above.) On completion of the aortic suture line, air was aspirated from the left heart, and the aortic cross-clamp was removed. At that time, instillation of cold saline solution into the pericardial cavity was discontinued in the SM group and the CJ was removed in the CJ group.
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Fig 1. . Cooling jacket—left atrial suture line. The patient's head is to the viewer's left. The posterior row of the left atrial suture line (lower portion of figure) has just been completed. The edge of the cooling jacket can be seen at the left upper and right sides of the figure. Notice that the cooling jacket does not compromise exposure for atrial suturing.
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Fig 2. . Cooling jacket—pulmonary suture line. The patient's head is to the viewer's left. The anterior row of the pulmonary artery suture line is about to be initiated. The cooling jacket, as seen in the upper portion of the figure, completely encompasses the left and right ventricular surfaces, minimizing external rewarming.
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Temperature Measurements and Statistical Methods
After removal from the transport device, donor hearts were placed in a container of refrigerated saline solution. The heart was trimmed for implantation and temperature probes were placed in the heart at three locations as previously described [5]. A 7-mm probe with thermocouples near the tip and hub was placed in the anterior right ventricle. A probe measuring 15 mm, also containing two thermocouples, one near the hub and another near the tip, was placed in the inferior aspect of the left ventricle. A single probe measuring 25 mm and containing a single thermocouple at the tip was placed in the left ventricular apex and positioned in the interventricular septum. Consequently, temperatures were measured at five ventricular sites: (1) anterior right ventricular epicardium, (2) right ventricular myocardium or cavity at a depth of 7 mm, (3) inferior left ventricular epicardium, (4) left ventricular myocardium or cavity at 13 mm, and (5) septum at 25 mm.
Beginning before implantation of the donor heart, temperatures at all five sites were registered with a computerized recording system (Cole-Parmer 8109 Temperature Data Logger, Chicago, IL). For comparison purposes temperatures were recorded before removal of the donor heart from the refrigerated saline container and every 30 seconds from the beginning of suturing of the left atrium until completion of the aortic suture line immediately before aortic cross-clamp removal. Comparisons of temperatures were made within and between the groups at each temperature site with respect to the minimum observed, maximum observed, and mean of the temperatures recorded during the monitoring period described above. Additionally, the percent of monitoring time that the temperature was 15°C or greater was compared. Temperatures were compared within and between the two groups at each site with a two-factor analysis of variance with group CJ as one factor and site as a repeated measures factor [9]. When the interaction between group and site was significant, groups were compared at each site with a modified t test [10]. Temperatures are presented as mean temperatures with standard deviation of the respective group at each of the five sites (Table 1).
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Results
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Before cardiac implantation and after probe placement, temperatures at all sites ranged between 6.0° and 9.0°C in both groups and were not significantly different. There were no significant temperature differences within the respective groups during implantation. However, the mean minimum temperature was significantly greater in the SM group than in the CJ group only at the left ventricular epicardial site. Also, the mean maximum temperature reached was higher in the SM group at all sites except the septum. Mean temperature was greater in the SM group at the left ventricular epicardial and myocardial sites. Similarly, the percentage of time that temperatures were 15°C or greater was significantly greater in the SM group versus the CJ group at the left ventricular epicardial and myocardial sites. Consequently, temperatures were higher in the SM group at the left ventricular epicardial site for all four comparisons and at the left ventricular myocardial site for the maximum, mean, and temperature of 15°C or greater comparisons (see Table 1
). A representative example of the temperature curves at all sites during cardiac implantation for the SM group is illustrated in Figure 3, whereas temperature curves for the CJ group are seen in Figure 4.
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Fig 3. . Typical temperature curves with the Stanford method. After placement of the temperature probes, temperatures at all sites ranged from 6° to 9°C at time 0. In spite of saline irrigation at 4°C through the left atrium and myocardial surface cooling with saline solution, there is a steady increase of temperatures at all sites. This temperature rise is greatest at the inferior left ventricular epicardium (LVE) site because of contact of the left ventricular surface with the pericardium and rewarming from adjacent structures. (LVM = left ventricular myocardium; RVE = anterior right ventricular epicardium; RVM = right ventricular myocardium; SEP = septum.)
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Fig 4. . Typical temperature curves with the cooling jacket. Throughout the aortic cross-clamp period during implantation, temperatures at all sites remain within 1° or 2°C of the initial temperatures at time 0. Furthermore, there are no temperature gradients across the left or right ventricular walls. The increase in all temperatures at 50 minutes is secondary to aortic cross-clamp removal. (LVE = inferior left ventricular epicardium; LVM = left ventricular myocardium; RVE = anterior right ventricular epicardium; RVM = right ventricular myocardium; SEP = septum.)
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Suture times (from beginning of the left atrial suture line to aortic unclamping) were not significantly different (40.8 ± 10.5 versus 41.4 ± 6.7 minutes, SM versus CJ).
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Comment
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Myocardial Temperatures During Donor Organ Transportation
In 1977 distant donor procurement was initiated at both Stanford University [11] and The Medical College of Virginia [12]. The method of cardiac preservation during transportation was identical at both institutions: after the donor organ was obtained, with or without initial perfusion with a hypothermic cardioplegic solution, hearts were placed in bags filled with saline solution which, in turn, were transported in multiple bags of saline solution packed in ice (11, 12).
Since then, considerable speculation has arisen as to the most appropriate temperature for preservation of the donor heart. Although in these earlier reports temperatures were reported to be at 4°C, there were no descriptions of continuous, or even intermittent, temperature monitoring. More recently, Keon and colleagues [13] reported that function of human atrial trabeculae appeared to be better after preservation at 12°C than lower temperatures. There was significant suppression of atrial contractility at 1° and 4°C. Hendry and associates [14] found there were no differences in ventricular function in dog hearts preserved at 0° to 4°C compared with those preserved at 12°C. In a previous study Hendry and associates [15], using the above method, described temperatures of less than 1°C occurring in dog hearts after 2 hours of preservation, and temperatures of less than 0°C were reached after 3 hours. Based on these changes, Hendry and associates recommended continuous monitoring of myocardial temperature during transportation of the donor heart. Similarly, Nataf and colleagues [16] have advocated maintenance of the donor heart at 4° to 6°C during transport. Also, Wheeldon and associates [17] reported the use of an ``eutectoid'' cooling device to keep temperatures at 4°C. Even Buckberg [18] concurs that, ``Deep hypothermia is an essential component of the storage process because it reduces metabolic rate and avoids the cumbersome need for continuous organ perfusion.'' Numerous other authors have confirmed that temperatures between 0° and 4°C do not appear to significantly compromise ventricular function after variable periods of preservation [19–23]. Continuous perfusion of the coronary arteries also has been reported as a method of transporting the donor heart but currently is used infrequently [24].
Myocardial Temperatures During Implantation
Because profound hypothermia (0° to 4°C) is the primary component of myocardial protection during transport of the donor heart, it seems especially important to assess and control myocardial temperatures during implantation. This consideration is probably even more important when donor heart ischemic times exceed 2 hours. Temperature changes at multiple sites of the myocardium during aortic cross-clamping have been reported for valve replacement [4] and coronary bypass grafting [7]; here, we have addressed temperature changes during implantation of the donor heart. Surprisingly, temperatures of these donor hearts increased to 6° to 9°C after they were transferred to a smaller bowl of saline solution, presumably at 4°C, where the probes were positioned in the myocardium. This finding emphasizes the importance of temperature monitoring of the donor heart during implantation. Although left atrial irrigation may, to some degree, neutralize the effects of rewarming due to continuous bronchial artery blood flow, the level of myocardial hypothermia must be measured. Furthermore, with irrigation of the left atrium, there is obvious mixing of return bronchial blood flow with the hypothermic saline solution. Aspiration and disposal of the saline solution may result in loss of blood. As well, additional hemodilution may occur if the solution is returned to the perfusate via cardiotomy suction.
In the present study the use of a CJ, without cold saline irrigation of the left atrium, resulted in significantly lower temperatures at the left ventricular epicardium with respect to lowest temperature obtained as well as maximum, mean, and percent of time temperatures were 15°C or greater. As previously pointed out by Swanson and co-workers [19], rewarming of the left ventricle during implantation occurs because of contact of the left ventricular surface with the pericardium allowing conduction of heat from adjacent cardiac structures. This direct contact prevents saline solution from circulating over the dependent left ventricular surface. The CJ precludes heat transfer by direct contact.
The fact that the left ventricular myocardial or cavity temperatures are not adequately maintained by cold saline solution irrigation of the left atrium is evidenced by temperatures that were 19.4° versus 13.7°C (SM versus CJ) for the maximum temperature reached, 22.9 versus 6.8° (SM versus CJ) for the percent of time temperatures were greater than 15°C, and the mean temperatures maintained (12.8° versus 10.3°C; SM versus CJ). A possible explanation for this is that mixing of the cold saline solution with the left atrial return blood flow or bronchial flow results in an increase in temperature of the saline/blood mixture entering the left ventricular cavity.
The maximum temperatures reached were also significantly greater at both right ventricular sites with the SM compared with the CJ (17.4° versus 13.9°C and 16.7° versus 13.6°C for right ventricular epicardium and myocardium, respectively). This suggests that uneven distribution of cold saline solution over the right ventricular surface results in uneven and inconsistent cooling [25]. Only the septal temperatures were not significantly different with respect to the four categories of temperatures assessed. Perhaps this was due to the fact that the relatively short implantation times (40.8 ± 10.5 minutes) did not allow sufficient time for rewarming of the septum in the SM group.
Alternatively, the use of multidose cardioplegia was advocated initially by Hardesty and colleagues in 1983 [26]. More recently Swanson and associates [19] and Nataf and colleagues [16] have advocated the use of multidose cardioplegia during implantation. Both Hardesty and colleagues [26] and Swanson and associates [19] have described better results in early cardiac function than with hypothermia alone but they did not report the changes of myocardial temperatures by cardioplegia.
Inferences
These temperature determinations suggest that if hypothermia of the myocardium is being relied on during cardiac implantation as the primary mode of myocardial protection, the use of a CJ rather than the SM will provide more consistent and deeper myocardial hypothermia. Furthermore, the potential loss of blood mixed with aspirated saline solution is eliminated as well as the possibility of the saline solution being aspirated by the cardiotomy suction devices and further diluting the perfusate.
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Acknowledgments
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We express our deep appreciation to Elizabeth A. Gilpin, MS, Programmer Analyst at the University of California, San Diego, for her technical expertise in the development of the statistical analysis of this article.
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Footnotes
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Address reprint requests to Dr Daily, 8010 Frost St, Suite 501, San Diego, CA 92123.
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References
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- Shumway NE, Lower RR, Stofer RC. Selective hypothermia of the heart in anoxic cardiac arrest. Surg Gynecol Obstet 1959;109:750–4.[Medline]
- Baumgartner WA, Reitz BA, Oyer PE, Stinson EB, Shumway NE. Cardiac homotransplantation. Curr Probl Surg 1979;16(9):6–61.
- Stiles QR, Hughes RK, Lindesmith GG. The effectiveness of topical cardiac hypothermia. J Thorac Cardiovasc Surg 1977;73:176–80.[Abstract]
- Daily PO, Pfeffer TA, Wisniewski JB, et al. Clinical comparisons of methods of myocardial protection. J Thorac Cardiovasc Surg 1987;93:324–36.[Abstract]
- Kinney TB, Daily PO, Pfeffer TA. Optimizing myocardial hypothermia: I. Temperature probe design and clinical inferences. Ann Thorac Surg 1991;51:278–83.[Abstract/Free Full Text]
- Daily PO, Kinney TB. Optimizing myocardial hypothermia: II. Cooling jacket modifications and clinical results. Ann Thorac Surg 1991;51:284–9.[Abstract/Free Full Text]
- Daily PO, Jones BH, Folkerth TL, Dembitsky WP, Moores WY, Reichman RT. Comparison of myocardial temperatures with multidose cardioplegia vs. single dose and myocardial surface cooling during coronary artery bypass grafting. J Thorac Cardiovasc Surg 1989;97:715–24.[Abstract]
- Baumgartner WA, Reitz BA, Stinson EB. Cardioplegia in human heart transplantation. In: Engelman RM, Levitsky S, eds. A textbook of clinical cardioplegia. New York: Futura, 1982:373–80.
- Winer BJ. Statistical principles and experimental design. New York: McGraw-Hill, 1971:514.
- Wallenstein S, Zuker CL, Fleiss J. Some statistical methods used in circulation research. Circ Res 1980;47:1–9.[Abstract/Free Full Text]
- Watson DC, Reitz BA, Baumgartner WA, et al. Distant heart procurement for transplantation. Surgery 1979;86:56–9.[Medline]
- Thomas FT, Szentpetery SS, Mammana RE, Wolfgang TC, Lower RR. Long-distance transportation of human hearts for transplantation. Ann Thorac Surg 1978;26:344–50.[Abstract/Free Full Text]
- Keon WJ, Hendry PJ, Taichman GC, Mainwood GW. Cardiac transplantation: the ideal myocardial temperature for graft transport. Ann Thorac Surg 1988;46:337–41.[Abstract/Free Full Text]
- Hendry PJ, Anstadt P, Plunkettt MD, et al. Optimal temperature for preservation of donor myocardium. Circulation 1990;82(Suppl 4):306–12.
- Hendry PJ, Walley VM, Koshal A, Masters RG, Keon WJ. Are temperatures attained by donor hearts during transport too cold? J Thorac Cardiovasc Surg 1989;98:517–22.[Abstract]
- Nataf P, Pavie A, Bracamontes L, Bors V, Cabrol C, Gandjbakhch I. Myocardial protection by blood cardioplegia and warm reperfusion in heart transplantation. Ann Thorac Surg 1992;53:525–6.[Abstract/Free Full Text]
- Wheeldon DR, Wallwork J, Bethune DW, English TAH. Storage and transport of heart and heart-lung donor organs with inflatable cushions and eutectoid cooling. J Heart Transplantation 1988;7:265–8.[Medline]
- Buckberg GD. Invited letter concerning: phases of myocardial protection during transplantation. J Thorac Cardiovasc Surg 1990;100:61–3.
- Swanson DK, Myerowitz D, Watson KM, Hegge JO, Fields BL. A comparison of blood and crystalloid cardioplegia during heart transplantation after 5 hours of cold storage. J Thorac Cardiovasc Surg 1987;93:687–94.[Abstract]
- Shragge BW, Digerness SB, Blackstone EH. Complete recovery of the heart following exposure to profound hypothermia. J Thorac Cardiovasc Surg 1981;81:455–8.[Abstract]
- Kao RL, Conti VR, Williams EH. Effect of temperature during potassium arrest on myocardial metabolism and function. J Thorac Cardiovasc Surg 1982;84:243–9.[Abstract]
- Rosenfeldt FL. The relationship between myocardial temperature and recovery after experimental cardioplegic arrest. J Thorac Cardiovasc Surg 1982;84:565–6.
- Harlan BJ, Ross D, Macmanus Q, Knight R, Luber J, Starr A. Cardioplegic solutions for myocardial preservation: analysis of hypothermic arrest, potassium arrest, and procaine arrest. Circulation 1978;58(Suppl 2):114–8.
- Wicomb WN, Cooper DKC, Novitzky D, Barnard CN. Cardiac transplantation following storage of the donor heart by a portable hypothermic perfusion system. Ann Thorac Surg 1984;37:243–8.[Abstract/Free Full Text]
- Rosenfeldt FL, Watson DA III. Local cardiac hypothermia: experimental comparison of Shumway's technique and perfusion cooling. Ann Thorac Surg 1979;27:17–23.[Abstract/Free Full Text]
- Hardesty RL, Griffith BP, Deeb GM, Bahnson HT, Starzl TE. Improved cardiac function using cardioplegia during procurement and transplantation. Transplant Proc 1983;15: 1253–55.[Medline]
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Abstract
Introduction
