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Ann Thorac Surg 1998;65:449-453
© 1998 The Society of Thoracic Surgeons

Original Articles: Cardiovascular

Retrograde Coronary Perfusion: Effects on Iatrogenic Edema and Diastolic Properties

David A. Dean, MD, Chao-Xiang Jia, MD, Santos E. Cabreriza, MBA, Pablo F. Soto, MD, David G. Rabkin, BA, Michael J. Sardo, BA, Natalya Chalik, BA, Henry M. Spotnitz, MD

Department of Surgery, Columbia University, College of Physicians and Surgeons, New York, New York, USA

Accepted for publication August 12, 1997.

Dr Spotnitz, Department of Surgery, Columbia University, College of Physicians and Surgeons, 622 W 168th Street, New York, NY 10032.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Background. The relative merits of antegrade infusion and retrograde infusion of cardioplegic solution in terms of heart weight, myocardial water content, and ventricular diastolic properties are undefined. Accordingly, we compared antegrade and retrograde flow of hemodiluted blood in isolated, hypothermic porcine hearts.

Methods. After cardiectomy, 1 L of cold heparinized blood diluted with lactated Ringer’s solution to concentrations ranging from 100% lactated Ringer’s to 50% lactated Ringer’s and 50% blood was perfused in an antegrade (n = 6) or retrograde (n = 6) fashion at mean pressures of 62 ± 2 mm Hg (± standard error of the mean) and 49 ± 2 mm Hg, respectively. Heart weight, myocardial water content, and left ventricular pressure–volume relationships were obtained before and after perfusion.

Results. In the comparison of measurements before and after perfusion, changes in heart weight (36 ± 4 g versus 5 ± 2 g; p < 0.05), myocardial water content (6.9% ± 1.0% versus 2.5% ± 0.4%; p < 0.01), and ventricular filling measured by normalized left ventricular volume at 10, 15, and 20 mm Hg were greater in the antegrade group.

Conclusions. In the isolated porcine heart, retrograde flow is distinguished from antegrade flow by less change in heart weight and myocardial water content and no diastolic dysfunction.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Optimal myocardial protection requires adequate delivery and distribution of cardioplegia. Relative merits have been identified with respect to type of cardioplegia (blood versus crystalloid), temperature (hypothermic versus normothermic), and mode of delivery (antegrade versus retrograde). Antegrade delivery of crystalloid cardioplegia has been associated with increases in myocardial water [1] [2] [3]. Myocardial edema has been demonstrated to cause increased diastolic stiffness of the left ventricle, which returns to normal with resolution of the edema [4]. Retrograde delivery of cardioplegia by way of the coronary sinus, as described by Pratt in 1898 [5], has gained clinical support for its ability to protect areas of myocardium distal to critical coronary stenoses [6] [7] [8]. Disadvantages include nonhomogeneous distribution, inferior protection of the right ventricle, and potential coronary sinus injury [8] [9].

Using methods established in vitro [2] [3], the present study examines effects of antegrade versus retrograde delivery of hemodiluted blood on the production of myocardial edema and the changes in left ventricular (LV) compliance. Effects of perfusate osmolarity on flow were also examined. Results indicate that delivery of cardioplegia by way of the coronary sinus minimizes myocardial edema and avoids adverse effects on LV diastolic properties.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Experimental Protocol
Animals received humane care in compliance with the "Principles of Laboratory Animal Care" formulated by the Institute of Laboratory Animal Resources and the "Guide for the Care and Use of Laboratory Animals" published by the National Institutes of Health (NIH publication 85-23, revised 1985). In addition, this study also conforms with the position of the American Heart Association on research animal use.

The protocol was carried out in conditioned Yorkshire pigs weighing 40 to 50 kg. An antegrade group (n = 6) and a retrograde group (n = 6) were anesthetized with acepromazine maleate (0.5 mg/kg intramuscularly), ketamine hydrochloride (20 mg/kg intramuscularly), and atropine sulfate (1 to 2 mg intramuscularly). After intubation, animals were mechanically ventilated, and arterial blood gas values were kept within physiologic norms. Anesthesia was maintained with isoflurane (1.75% to 2.00%) in oxygen. A median sternotomy was performed while the electrocardiogram, peripheral arterial blood pressure, and body temperature were monitored. After pericardiotomy, the inferior and superior venae cavae, the pulmonary artery, and the aorta were isolated with snares. The left hemiazygos vein, which drains directly into the coronary sinus in pigs [10], was identified and ligated.

Pigs were systemically heparinized (300 IU/kg); arterial whole blood was removed and added to cold (4°C) lactated Ringer’s solution (274 mOsm/L) to produce perfusates of 100% (n = 2), 75% (n = 1), 67% (n = 2), and 50% lactated Ringer’s solution (n = 1). Hearts were arrested as follows: the venae cavae were snared; the pulmonary veins were incised to decompress the heart; the aorta was cross-clamped; and 60 mEq of cold potassium chloride solution was infused into the aortic root. Hearts were then rapidly excised and placed in a slurry of blood and frozen lactated Ringer’s solution. Each heart was blotted dry and weighed (Ohaus Scale Corp, Florham Park, NJ) for determination of heart weight (HW) before perfusion. Myocardial biopsy specimens from the left and right ventricles were removed for determination of myocardial water content (MWC).

A 5F catheter was placed in the apex of the left ventricle with a pursestring suture for pressure monitoring and volume infusion. A 5F micromanometer (Millar Instruments, Houston, TX) was attached to the catheter by a three-way stopcock. The mitral annulus was sealed with a Satinsky clamp across the atrioventricular groove, and the aorta was similarly sealed by placing a clamp close to the aortic annulus, thus occluding the coronary ostia. Zero pressure was defined at midlevel of the submerged left ventricle. Cold fluid from the slurry was then infused into the sealed left ventricle in 5-mL increments at intervals of 3 to 5 seconds, while digitized (MacLab; AD Instruments Inc, Milford, MA) pressure was simultaneously recorded on a digital computer (Macintosh Quadra 950; Apple Computer, Cupertino, CA). Pressure–volume data were recorded from zero volume to 20 mm Hg; data were valid only if at least 95% of the infused volume was recovered. Pressure–volume data were measured in duplicate and averaged. The Satinsky clamp was then removed in preparation for perfusion.

In the antegrade group, a cardioplegia needle (with a pressure-monitoring port) was placed proximal to the aortic cross-clamp, and 1 L of hemodiluted perfusate was infused at a pressure of 60 to 70 mm Hg (mean pressure, 62.5 ± 2.2 mm Hg). In the retrograde group, a suture was circumferentially placed around the coronary sinus and a Foley catheter was placed into this sinus. The balloon was inflated, the pursestring suture was snared down, and the balloon was pulled back against the ostium snugly to avoid occlusion of right ventricular veins draining into the coronary sinus. One liter of hemodiluted perfusate was infused at a pressure of 40 to 50 mm Hg (mean pressure, 49 ± 2 mm Hg). After perfusion, hearts from both groups were blotted and weighed to determine HW after perfusion. Clamps were placed across the atrioventricular groove and the aortic annulus, and pressure–volume data were recorded in duplicate and averaged. Myocardial biopsy specimens from the right and left ventricles were removed for MWC determination.

Data Analysis
Samples for MWC were blotted dry and weighed (type H16 analytical balance; Mettler Instruments Corp, Hightstown, NJ) to obtain wet weight; each specimen was then dried to a constant weight in an oven at 60°C for 48 hours. Water content percentage was then calculated as follows:

Mean preperfusion HW was 166 ± 3 g. For comparison of volume data between hearts of different sizes, LV volumes were normalized to an HW of 166 g with the following formula:

In addition, for comparisons between groups, pressure–volume data were analyzed by dividing the data into six 5-mm Hg increments of pressure from -5 mm Hg to 20 mm Hg. Pressure and volume were averaged for each interval and plotted. Graphic analysis of LV pressure–volume relationships consisted of exponential curve fitting (IGOR; Wavemetrics, Inc, Lake Oswego, OR) of pressure (P) and volume (V) by the least squares method: P={alpha}eßV, where ß is the LV stiffness constant, and {alpha} is the base constant.

Statistical Methods
Mean HW, MWC, and filling volumes for both groups after perfusion were compared with the preperfusion values by analysis of variance. Post-test statistical significance was calculated using Tukey’s multiple comparisons test. Analysis of covariance was used to determine the effect of dilution and direction of perfusion on each variable. Time, pressure, volume, flow, and perfusate osmolarity for antegrade perfusion were compared with the comparable variables for retrograde perfusion by Student’s t test. Corresponding test statistics were considered significant at a level with a p value of less than 0.05.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
Mean perfusion data are presented in Table 1. Antegrade perfusion was faster than retrograde perfusion (150 ± 31 seconds versus 910 ± 132 seconds; p < 0.01). Perfusion pressure, maintained at clinical levels, was higher in the antegrade group (63 ± 1 mm Hg versus 49 ± 1 mm Hg; p < 0.01). Calculated flow resistance, estimated from mean data in Table 1 was 4.8 times greater in the retrograde group than in the antegrade group. Mean osmolarity for the groups was not different.


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  		Summary of Perfusion Data for Antegrade and Retrograde Perfusion Groups1

 
Mean HW, MWC, and passive filling properties are shown in Table 2. After perfusion, the antegrade group was characterized by significant (p < 0.05) increases in HW (203 ± 5 g versus 168 ± 4 g) and MWC (84.2% ± 0.8% versus 77.3% ± 0.2%). Filling volume at 10, 15, and 20 mm Hg decreased significantly after perfusion in the antegrade group. The observed changes were significantly different (p < 0.05) from those in the retrograde group. Of the variables tabulated, only MWC changed significantly after perfusion in the retrograde group (80.5% ± 0.4% versus 77.9% ± 0.3%; p < 0.05).


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  		Mean Heart Weight, Water Content, and Passive Filling Volumes for Antegrade and Retrograde Coronary Perfusion1

 
Effects of perfusion on diastolic properties are illustrated in Fig 1. Antegrade perfusion is associated with a shift upward and to the left of the mean pressure–volume curve for diastolic filling. Minimal changes occur after retrograde perfusion.



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  		Effects of antegrade and retrograde perfusion on pressure–volume relationship in isolated arrested left ventricle (LV). Pressure and normalized volume were averaged for data grouped into pressure intervals averaging 0, 5, 10, 15, and 20 mm Hg (see text). An additional data point was obtained by averaging pressure at zero volume. With antegrade perfusion, filling volume after (Post) perfusion was significantly lower at pressures averaging 10, 15, and 20 mm Hg. Standard errors are indicated by brackets. (Pre = before.)

 
Fig 2 illustrates effects of perfusate dilution on HW. Heart weight significantly increased with hemodilution after antegrade perfusion, but no effect was noted after retrograde perfusion (analysis of variance, p < 0.05).



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  		Relation between perfusate dilution and change in heart weight (HW) after perfusion. Change in HW increased linearly with hemodilution after antegrade perfusion, whereas no effect of osmolarity on HW was observed after retrograde perfusion. The difference between the antegrade and retrograde groups is significant by analysis of covariance.

 
Fig 3 illustrates effects of perfusate dilution on LV filling volume at 15 mm Hg filling pressure. Filling volume decreased as hemodilution increased in the antegrade group. No relation between hemodilution and changes in diastolic properties was apparent in the retrograde group.



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  		Relation between perfusate dilution and change in filling volume at 15 mm Hg filling pressure (LVV-15). Changes in LVV-15 after antegrade perfusion were directly related to perfusate hemodilution, but no effect of osmolarity on LVV-15 was observed after retrograde perfusion. The difference between the antegrade and retrograde groups is significant by analysis of covariance.

 
The relation between HW and filling volume at 15 mm Hg filling pressure is illustrated in Fig 4. An increase in HW is associated with a decrease in filling volume; there is no apparent difference in this relationship for the antegrade and retrograde groups. The correlation coefficient is 0.93. Correlation coefficients from linear regression analysis of MWC versus HW and versus LV filling volume at 15 mm Hg filling pressure were 0.90 and 0.79, respectively.



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  		Relation between change in heart weight and change in filling volume at 15 mm Hg filling pressure (LVV-15) for all animals in study. Heart weight was closely related to changes in compliance (correlation coefficient = 0.93). This relation did not appear to be affected by type of perfusion, either retrograde or antegrade. (LV = left ventricle; WHW = wet heart weight.)

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
This study demonstrates that, in the hypothermic porcine heart, antegrade coronary perfusion is distinguished from retrograde perfusion by faster flow, greater increases in HW and MWC, and greater decreases in passive LV filling volume at three levels of LV pressure. Hemodilution did not affect HW or filling volume after retrograde perfusion. However, after antegrade perfusion, increasing hemodilution magnified increases in HW and decreases in LV filling volume.

These results appear to define advantages for the use of retrograde cardioplegia administration beyond those recognized previously. However, this study involved primarily diluted blood without additives commonly used for clinical cardioplegia. The diluent employed, lactated Ringer’s solution, is somewhat atypical of what is used to prepare clinical cardioplegic solutions. In addition, the complexity of the protocol was augmented by the use of a spectrum of perfusates, including perfusates quite atypical of those employed clinically. A discussion of additional sources of possible experimental error and deviation from the clinical setting follows.

The results could have been affected by some form of flow obstruction peculiar to the model employed; although flow rates for retrograde cardioplegia as low as 30 mL/min have been reported [11], 200 mL/min is commonly recommended for retrograde flow [12] and 250 to 350 mL/min is currently suggested for antegrade flow [13]. Technical factors related to catheter position do not appear to have been involved, and coronary sinus valves are not known to affect retrograde flow in pigs. The observed flow resistance in the model used here was nearly five times greater in the retrograde group than in the antegrade group.

Nonnutritive coronary flow with retrograde perfusion [14] [15] [16] is also problematic in studies of antegrade and retrograde flow, as it tends to augment flow as a result of precapillary shunting. Partington and co-workers [14] demonstrated with radioactive microspheres that nutritive flow in the left ventricle averaged 65% by retrograde perfusion versus 87% by antegrade perfusion. Aldea and associates [15] showed with radiolabeled microspheres that antegrade delivery of cardioplegia achieved significantly greater nutritive flow than retrograde delivery (1.37 ± 0.31 mL · g-1 · min-1 versus 0.39 ± 0.09 mL · g-1 · min-1).

Because venovenous shunting occurs through thebesian veins with coronary sinus perfusion, microsphere size is important in calculating flow; cardioplegic solution can be shunted from capillaries distal to microsphere entrapment. Villanueva and colleagues [16] used radioisotopes of thallium 201 and technetium 99m sestamibi to determine flow because this technique requires capillary penetration prior to cellular uptake. The group demonstrated that microspheres tended to overestimate capillary flow. Retrograde flow was considerably less than antegrade flow using these radioisotopes.

Another possible mechanism for differences in the antegrade and retrograde perfusion groups involves perfusion pressure. We chose to keep the retrograde pressure as close to clinical standards as possible. The fact that antegrade perfusion with 50% hemodiluted blood did not cause significant alterations in MWC and diastolic properties supports the conclusion that in this model, osmolarity had a greater effect on extravasation of water than pressure. Thus, both decreased capillary perfusion and lower perfusion pressure may have contributed to decreased myocardial edema after retrograde perfusion. Similar effects may occur clinically.

The changes observed in LV passive properties in the antegrade group were similar to results previously reported from our laboratory [2] [3]. Fig 4 demonstrates that as HW increased, a result of increased myocardial water, passive filling decreased, as represented by smaller LV filling volume at 15 mm Hg filling pressure. The mechanism relating myocardial edema to decreased filling volume has been a subject of speculation [17] [18]. Detwiler and associates [19] demonstrated an increase in the linear stiffness of papillary muscle after perfusion-induced edema, which might explain the alterations in diastolic properties after antegrade perfusion. Increased longitudinal cell stiffness, damage to the collagen matrix, and interference with cellular rearrangement during ventricular filling may also contribute to stiffness [20]. Studies from our laboratory [21] [22] have previously found that changes in passive filling properties observed in vitro in edematous states accurately predict alterations in diastolic properties observed in the beating heart.

In the present study, MWC increased 7% after antegrade perfusion. Previous analysis [23] demonstrated that a 5% increase in water content is associated with a 50% increase in intracellular water. Thus, it is reasonable to expect that this increase in intracellular water would cause cell stiffness.

The present experiments were in isolated hypothermic hearts. Our hypothesis was that changes seen during the experiment occur in the absence of ischemia (ie, an intact vascular endothelium and undamaged myocardial cells). In actuality, the amount of ischemia is unknown, but previous studies [2] have demonstrated that LV compliance at 8°C does not change during a 90-minute period of ischemia. Furthermore, as there was no difference in total cold ischemia time between groups, ischemic contracture does not appear to be the primary mechanism for observed changes in LV diastolic properties.

The clinical significance of these findings needs further investigation. The results suggest that continuous retrograde perfusion during cardiac surgical procedures may not lead to increases in MWC or cause changes in diastolic properties. However, the effects of retrograde perfusion after ischemic injury were not investigated in this study, the heart was excised and profoundly hypothermic, and many other conditions differed substantially from the clinical environment.

We conclude that retrograde perfusion with hypoosmolar perfusates in the isolated hypothermic porcine heart is distinguished from antegrade perfusion by less myocardial edema and no diastolic dysfunction. Edema appears to be the primary cause of the observed changes in diastolic properties.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This study was supported in part by grant 1 RO1 HL-48109 from the US Public Health Service.

Doctor Dean was supported by the National Institutes of Health National Research Service Award training grant HL09325-01.

Doctor Spotnitz is the George H. Humphreys II Professor of Surgery.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Foglia RP, Steed DL, Follette DM Iatrogenic myocardial edema with potassium cardioplegia. J Thorac Cardiovasc Surg 1979;78:217-222.[Abstract]
  2. Weng ZC, Nicolosi AC, Detwiler PW, et al. Effects of crystalloid, blood, and University of Wisconsin perfusates on weight, water content, and left ventricular compliance in an edema-prone, isolated porcine heart model. J Thorac Cardiovasc Surg 1992;103:504-513.[Abstract]
  3. Hsu DT, Weng Z-C, Nicolosi AC, Detwiler PW, Sciacca R, Spotnitz HM Quantitative effects of myocardial edema on the left ventricular pressure–volume relation in the isolated stored pig heart. J Thorac Cardiovasc Surg 1993;106:651-657.[Abstract]
  4. Takoudes TG, Amirhamzeh MMR, Hsu DT, Wise BR, Odeh SO, Spotnitz HM Time course of resolution of perfusion-induced myocardial edema in the rat heart. J Surg Res 1994;57:641-646.[Medline]
  5. Pratt FH The nutrition of the heart through the vessels of Thebesius and the coronary veins. Am J Physiol 1898;1:86-103.[Free Full Text]
  6. Partington MT, Acar C, Buckberg GD, Julia PL Studies of retrograde cardioplegia. II. Advantages of antegrade/retrograde cardioplegia to optimize distribution in jeopardized myocardium. J Thorac Cardiovasc Surg 1989;97:613-622.[Abstract]
  7. Bolling SF, Flaherty JT, Bulkley BH, Gott VL, Gardner TJ Improved myocardial preservation during global ischemia by continuous retrograde coronary sinus perfusion. J Thorac Cardiovasc Surg 1983;86:659-666.[Abstract]
  8. Menasché P, Kural S, Fauchet M, et al. Retrograde coronary sinus perfusion: a safe alternative for ensuring cardioplegic delivery in aortic valve surgery. Ann Thorac Surg 1982;34:647-658.[Abstract]
  9. Hammond GL, Davies AL, Austen WG Retrograde coronary sinus perfusion: a method of myocardial protection in the dog during left coronary artery occlusion. Ann Surg 1967;166:39-47.[Medline]
  10. Gilbert SG The circulatory system. In: Gilbert SG, ed. Pictorial anatomy of the fetal pig, 2nd ed. Seattle: University of Washington Press, 1966:49.
  11. Menasché P, Piwnica AH Retrograde coronary sinus perfusion. In: Roberts AJ, ed. Myocardial protection in cardiac surgery. New York: Marcel Dekker, 1987:251-252.
  12. Vivek R, Weisel RD Intraoperative protection of organs: hypothermia, cardioplegia, and cerebroplegia. In: Edmunds LH, ed. Cardiac surgery in the adult. New York: McGraw-Hill, 1997:295-318.
  13. Buckberg GD, Allen BS Myocardial protection management during adult cardiac operations. In: Baue AE, Geha AS, Hammond GL, Laks H, Naunheim KS, eds. Glenn’s thoracic and cardiovascular surgery. Stamford, CT: Appleton and Lange, 1996:1653-1687.
  14. Partington MT, Acar C, Buckberg GD, Julia PL, Kofsky ER, Bugyi HI Studies of retrograde cardioplegia. I. Capillary blood flow distribution to myocardium supplied open and occluded arteries. J Thorac Cardiovasc Surg 1989;97:605-612.[Abstract]
  15. Aldea GS, Hou D, Fonger JD, Shemin RJ Inhomogeneous and complementary antegrade and retrograde delivery of cardioplegic solution in the absence of coronary artery obstruction. J Thorac Cardiovasc Surg 1994;107:499-504.[Abstract/Free Full Text]
  16. Villanueva FS, Spotnitz WD, Glasheen WP, Watson DD, Hayaweera AR, Kaul S New insights into the physiology of retrograde cardioplegia delivery. Am J Physiol 1995;268(4 Pt 2):H1555-H1566.
  17. Schaff HV, Gott VL, Goldman RA, Frederiksen JW, Flaherty JT Mechanism of elevated left ventricular end-diastolic pressure after ischemic arrest and reperfusion. Am J Physiol 1981;240:H300-H307.
  18. Spotnitz HM, Hsu DT Myocardial edema: importance in the study of left ventricular function. Adv Cardiac Surg 1994;5:1-25.[Medline]
  19. Detwiler PW, Nicolosi AC, Weng Z-C, Spotnitz HM Effects of perfusion-induced edema on stress-strain properties in the intact swine papillary muscle. J Thorac Cardiovasc Surg 1994;108:467-476.[Abstract/Free Full Text]
  20. Spotnitz HM, Spotnitz WD, Cottrell TS, Spiro D, Sonnenblick EH Cellular basis for volume-related wall thickness changes in the rat ventricle. J Mol Cell Cardiol 1974;6:317-331.[Medline]
  21. Amirhamzeh MMR, Dean DA, Jia C-X, et al. Iatrogenic myocardial edema: increased diastolic compliance and time course of resolution in vivo. Ann Thorac Surg 1996;62:737-743.[Abstract/Free Full Text]
  22. Dean DA, Jia C-X, Cabreriza SE, Amirhamzeh MMR, Soto PF, Spotnitz HM Does myocardial edema cause apparent myocardial depression in severe sepsis and trauma. Surg Forum 1996;47:56-58.
  23. Steenbergen C, Hill ML, Jennings RB Volume regulation and plasma membrane injury in aerobic, anaerobic, and ischemic myocardium in vitro: effects of osmotic cell swelling on plasma membrane integrity. Circ Res 1985;57:864-875.[Abstract/Free Full Text]



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