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Ann Thorac Surg 2003;78:506-512
© 2003 The Society of Thoracic Surgeons

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Original article: cardiovascular

A prospective randomized study to evaluate stress response during beating-heart and conventional coronary revascularization

^a Wessex Cardiothoracic Centre, Southampton, United Kingdom
^b Department of Endocrinology, Southampton General Hospital, Southampton, United Kingdom

Accepted for publication July 17, 2003.

^* Address reprint requests to Dr Velissaris, Wessex Cardiothoracic Centre, Southampton General Hospital, Tremona Rd, Southampton, SO16 6YD, UK.
e-mail: theo{at}velissaris.com

Presented at the Thirty-ninth Annual Meeting of The Society of Thoracic Surgeons, San Diego, CA, Jan 31–Feb 2, 2003.

	Abstract

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
BACKGROUND: Cardiopulmonary bypass (CPB) is associated with a systemic stress hormonal response, which can lead to changes in hemodynamics and organ perfusion. We examined perioperative stress hormone release in low-risk patients undergoing coronary artery bypass grafting with and without cardiopulmonary bypass.

METHODS: Fifty-two patients undergoing primary coronary artery bypass grafting by the same surgeon were randomly assigned into either on-pump (n = 26) or off-pump (n = 26) groups. The on-pump coronary artery bypass grafting group underwent mildly hypothermic (35°C) pulsatile cardiopulmonary bypass with arterial line filtration. Arterial blood samples were collected preoperatively, at the end of operation, and at 1, 6, and 24 hours postoperatively. Plasma levels of vasopressin and cortisol were measured using radioimmunoassay. Anesthetic management was standardized.

RESULTS: Both groups had similar demographic makeup and extent of revascularization (on-pump coronary artery bypass grafting, 2.8 ± 1.0 grafts versus off-pump coronary artery bypass grafting, 2.4 ± 0.9 grafts; p = 0.20). No mortality or major morbidity was observed and there were no crossovers. The cardiopulmonary bypass and aortic cross-clamp times in the on-pump coronary artery bypass grafting group were 63 ± 24 and 33 ± 11 minutes, respectively. In both groups there was a similar and significant rise in cortisol and vasopressin levels in the early postoperative phase, with a partial recovery toward baseline values observed at 24 hours postoperatively. Repeated measures analysis of covariance showed no significant difference between the groups with time for both hormones (cortisol, p = 0.40; vasopressin, p = 0.30).

CONCLUSIONS: Despite the avoidance of cardiopulmonary bypass, off-pump coronary artery bypass grafting surgery triggers a systemic stress hormone response that is comparable to conventional surgical revascularization. The neurohormonal environment during beating-heart surgery should be further explored.

	Introduction

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
Cardiopulmonary bypass (CPB) is associated with well-described changes in the neurohormonal environment, which are characterized by the activation of the sympathetic axis and a generalized stress endocrine response [1–5]. The stress response leads to the release of hormones that predominantly exert a catabolic action with resultant protein and fat mobilization, such as cortisol and glucagon, and hormones that primarily aim to retain fluid, such as vasopressin (or antidiuretic hormone) and aldosterone. Although not routinely measured in clinical practice, an evaluation of the magnitude of stress response is widely accepted as a research tool to assess the ability of different CPB or anesthetic protocols to achieve a more physiologic milieu during surgery [6–9]. Despite a lack of data to demonstrate an association between stress response and clinical outcome, it is generally accepted that techniques that attenuate the stress response are likely to be better tolerated with preservation of perioperative organ function.

The stress hormonal response to CPB is not unique, representing a universal response to surgery, trauma, and other types of injury, such as burns [10, 11]. The neurohormonal environment during off-pump coronary artery bypass grafting (OPCAB), which is now an established modality for the surgical treatment of coronary artery disease, has not so far been investigated. Although it appears logical that avoidance of CPB should provide a more physiologic milieu, the possible advantages or disadvantages of OPCAB need to be carefully evaluated. Some of the physiologic alterations described in open heart surgery may primarily be caused by the effect of general anesthesia and major surgery on patients with coronary artery disease, who often have significant comorbidities. Pertinent to this is the fact that several studies have shown no advantage of OPCAB versus surgery with CPB in the perioperative function of organs such as the lung, the brain, and the kidneys [12–14]. The purpose of this study was to evaluate in a prospective randomized study the stress hormonal response in low-risk patients undergoing coronary vascular surgery with or without CPB.

	Patients and methods

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
Study design
Fifty-two patients undergoing primary elective coronary artery bypass grafting who satisfied the study criteria (Table 1) were prospectively recruited after informed consent. The study was approved by our institution's local research ethics committee. Essentially we studied low-risk patients with no history of endocrine disease and normal preoperative cardiac function. All patients were operated on by the same surgeon (S.K.O.), and there were no contraindications to OPCAB after review of the preoperative coronary angiogram. The patients were randomized the day before the operation into either surgery with CPB (ONCAB group, n = 26) or off-pump surgery (OPCAB, n = 26) by simple randomization using a table of random numbers.

Target hemodynamic values perioperatively in both groups were mean arterial pressure greater than 60 mm Hg and cardiac index greater than 2.2 L · min^–1 · m^–2 (hemodynamic management during CPB is outlined below). Invasive monitoring included continuous cardiac output monitoring using a Swan-Ganz catheter (Edwards Lifesciences LLC, Irvine, CA) inserted through the right internal jugular vein after anesthetic induction. Target hemodynamics were generally obtained by optimizing preload followed by the use of inotropic support or vasoconstrictors as indicated. Dopamine was used as the first-line inotropic agent, whereas bolus intravenous injections of phenylephrine or norepinephrine infusion were used as vasoconstrictors.

Cardiopulmonary bypass management
A standardized CPB protocol was used for the ONCAB patients. Cardiopulmonary bypass was established using bicaval cannulation with two individual cannulas to the superior and inferior vena cava and an arterial cannula (Medtronic DLP; Medtronic Ltd, Watford, UK) placed in the ascending aorta. Pulsatile CPB was conducted under mild core hypothermia (35°C), using a hollow-fiber membrane oxygenator (D903 Avant; Sorin Biomedica, Mirandola, Italy) and arterial line filtration (D734 Micro 40; Sorin Biomedica). The circuit was primed with 1 L of Hartman's solution, 500 mL of Gelofusine and 5,000 IU of sodium heparin. Intermittent antegrade cold-blood cardioplegia (4°C) delivered through a 12-gauge aortic root cannula was used for myocardial protection. The cardioplegic mixture consisted of 20% St. Thomas' Hospital No. 2 solution (Martindale Pharmaceuticals, Essex, UK) and 80% autologous blood. A dose of 12 mL/kg was delivered to induce diastolic cardiac arrest and a maintenance dose of 3 mL/kg was administered after completion of each distal anastomosis. The left ventricle was vented through the aortic root during aortic cross-clamping. Flow was maintained at 2.5 L · min^–1 · m^–2 during CPB with judicious use of phenylephrine and phentolamine to maintain the mean perfusion pressure between 50 and 80 mm Hg. Alpha-stat management of acid-base status was used. Proximal graft anastomoses on the ascending aorta were performed after aortic cross-clamp removal using a partially occlusive clamp.

Off-pump coronary artery bypass grafting technique
A median sternotomy was used for surgical access in all cases. Partial systemic heparinization was used with a target activated clotting time of 300 to 400 seconds before cardiac manipulation. Trendelenburg posture was used throughout the period of distal anastomoses, and a single suture technique [15] was used to facilitate exposure of the target coronary arteries. A mechanical suction-based myocardial tissue stabilizer (Octopus3; Medtronic Ltd) was used to immobilize the operative field during coronary anastomosis. After arteriotomy, an intraluminal coronary shunt (Flo-Thru; Biovascular Inc, Minnesota, MN) was inserted to maintain distal myocardial perfusion and was removed before completion of the anastomosis. Core temperature was maintained at or above 35°C throughout the procedure by minimizing heat loss and using active warming techniques. Hemodynamic stability was achieved primarily with preload management (intravenous fluid administration and Trendelenburg posture) and vasoactive agents as required. Construction of the proximal anastomoses to the ascending aorta was performed within a single aortic side-biting clamp period, with the systolic arterial pressure was maintained at100 mm Hg or greater to minimize aortic trauma.

Vasopressin and cortisol levels
Blood samples were collected from the radial artery into ethylenediaminetetraacetic acid –containing glass tubes shortly after anesthetic induction, at the end of operation, and 1, 6, and 24 hours postoperatively. The samples were immediately centrifuged in a refrigerated centrifuge at 3,000 g for 10 minutes to separate the plasma, which was subsequently frozen and stored at –70°C until assayed. Levels of vasopressin were measured using a commercially available radioimmunoassay (Vasopressin 100T Kit; Nichols Institute Diagnostics, San Juan Capistrano, CA). The interassay coefficient of variance was calculated in our laboratory at 8.4% (n = 8). The observed range of plasma values is 0 to 8 ng/L. Cortisol levels were measured using a routinely available in-house developed radioimmunoassay (interassay coefficient of variance, 9.1%, n = 14; reference range 8 to 10 am, 150 to 750 nmol/L) [16].

Statistical analysis
The results are expressed as the mean ± standard deviation or median with interquartile range for nonnormally distributed variables. Patient characteristics and perioperative clinical data in the two groups were compared using a two-sample Student's t test or a Mann-Whitney U test if normal distribution could not be assumed. Categorical variables were compared using the Pearson's ²or Fisher's exact test as appropriate. Repeated measures analysis of covariance, with the baseline measurement as a covariate, was used to assess the effect of time, group, and group–time interaction on outcome. A paired Student's t test was used for intragroup comparison between individual points. To investigate any possible associations between the extent of cortisol or vasopressin release and clinical outcome, the area under the curve for the levels of cortisol and vasopressin as a function of time was calculated using the method described by Matthews and colleagues [17]. Because the data contained subgroups (ONCAB versus OPCAB), Spearman's rank correlation analysis was used to investigate the association between the extent of hormone release and clinical outcome variables, whereas logistic regression was used for binary outcome variables. The Statistical Package for Social Sciences (SPSS) version 10.1 software was used for all descriptive statistics and inferential testing. A p value of less than 0.05 was considered statistically significant.

	Results

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
Patient characteristics, operative data, and clinical outcome
All patients completed the study protocol and no patient assigned to the OPCAB group required the use of CPB. Preoperative patient characteristics are presented in Table 2. As explained in the Methods, these were low-risk cases and no significant differences between the groups were observed. Table 3 summarizes the intraoperative data and clinical outcome. The groups had a similar extent of revascularization and similar operation duration. There were no significant differences in the postoperative duration of mechanical ventilation or the time required for the patients to rewarm to a systemic (nasopharyngeal) temperature of 37°C. There were no differences between the groups in dopamine or norepinephrine usage or the development of a low cardiac output (cardiac index < 2.2 L · min^–1 · m^–2) perioperatively. There were no deaths and no patient required the use of intraaortic balloon pump. No major complications, such as myocardial infarction, major neurologic complications, or end-organ failure (other than transient low cardiac output) were observed. Table 4 summarizes the hemodynamic data in the two groups at the sampling points. Although in the early postoperative phase (end of operation and 1 hour postoperatively) there was a trend for the OPCAB patients to maintain superior cardiac output with less systemic vasoconstriction, there were no overall significant differences between the groups. Hemodynamic data at 24 hours postoperatively were not recorded as ethical considerations did not allow us to use Swan-Ganz catheter monitoring beyond 6 postoperative hours, unless it was clinically indicated.

View larger version (11K): [in this window] [in a new window]   Fig 1. Perioperative cortisol levels in the two groups. The error bars represent 95% confidence intervals around the mean (for clarity only the plus error bars are displayed for the off-pump coronary artery bypass grafting group and the minus for the on-pump coronary artery bypass grafting group). Solid line = on-pump (n = 26); broken line = off-pump (n = 26).

View larger version (11K): [in this window] [in a new window]   Fig 2. Perioperative vasopressin levels in the two groups. The error bars represent 95% confidence intervals around the mean (for clarity only the plus error bars are displayed for the off-pump coronary artery bypass grafting group and the minus for the on-pump coronary artery bypass grafting group). Solid line = on-pump (n = 26); broken line = off-pump (n = 26).

	Comment

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

Plasma hormone measurements during CPB can be difficult to interpret in the context of acute hemodilution at the onset of CPB [18, 21]. This issue has been debated for some time, and most authors suggest that no corrections should be made for hemodilution, as the concentration of a hormone in a target organ is directly affected by its concentration in the serum rather than the total amount in the intravascular fluid. The confounding factor of hemodilution is less relevant in the postoperative period, when the body has begun to compensate by redistributing the excess volume between its fluid compartments. Although it was not intended when the study was designed, we analyzed our results after correction for hemodilution as well (results not shown), and this did not alter the study findings.

Our findings of vasopressin and cortisol changes during OPCAB are not surprising if one considers that release of stress hormones is a fundamental part of the body response to surgery and major trauma [10, 11]. What is perhaps more interesting is the fact that the magnitude of hormonal changes was similar in the two groups. Given the randomized nature of the study design, the controlled anesthetic and analgesic protocol, and the absence of any significant differences in the preoperative characteristics and baseline hormone measurements of the two groups, these results may at first appear surprising. One would intuitively expect some benefit conferred by the avoidance of CPB. The only apparent difference between the groups that would explain the study findings are the inherent differences between OPCAB and CPB techniques and the limitations of each approach.

Cardiopulmonary bypass evokes a systemic inflammatory response through the exposure of blood to foreign surfaces with subsequent activation of various cellular and humoral elements. Several studies have shown an attenuation of the perioperative systemic inflammation with the OPCAB technique compared with CPB [22, 23]. However, recent evidence suggests that there is significant transient hemodynamic deterioration during distal anastomoses in OPCAB [24–27], so that the benefit of a reduced inflammatory response may have to be weighed against the potential for ischemic injury. Compared with the controlled systemic flow conditions of CPB, cardiac manipulation during OPCAB for the exposure of target coronary arteries leads to significant hemodynamic impairment, with transient drops in the cardiac output, despite relative preservation of the mean arterial pressure. It has been shown that the hemodynamic deterioration is primarily caused by right ventricular dysfunction, as a result of compression of the right heart chambers against the surrounding fibrous pericardium and pleura [24]. The hemodynamic changes are more pronounced when extensive cardiac manipulation is required to expose a target vessel on the posterior aspect of the heart, and are generally reversible once the heart is replaced in its normal position. It is conceivable that in terms of stress hormone response, the benefit conferred by avoiding CPB was negated by cumulative hemodynamic stress of OPCAB surgery.

Support for this explanation can be derived from a previous study investigating the pattern of vasopressin release during coronary artery bypass grafting with CPB and during thymectomy through median sternotomy [10]. Although plasma vasopressin levels were higher in the CPB group, a significant increase was also noticed during thymectomy. Interestingly, the increase in vasopressin was related to hemodynamic factors and surgical stimulation, such as median sternotomy and pericardial retraction. Further support for the central role of hemodynamic performance in stress response comes from several studies that have investigated the impact of pulsatile flow during CPB on hormone levels. The use of pulsatile flow during CPB results in a more physiologic hormonal environment perioperatively with attenuation of the stress hormone response compared with nonpulsatile CPB [3, 6, 28]. Pulsatile flow maintains capillary patency by delivering more energy into the vasculature and ameliorates the CPB-related rise in systemic vascular resistance by reducing the release of vasoconstrictors, such as angiotensin II [29]. However, other studies have not confirmed a beneficial effect of pulsatile perfusion on perioperative stress response [1, 19]; differences among various studies in the anesthetic protocols and other aspects of the CPB protocol, such as the systemic temperature, the flow level, and the pulsatile flow variables, may account for these discrepancies.

Systemic hypothermia during CPB has also been shown to attenuate perioperative stress hormone response [30, 31], although in one study there was no difference in vasopressin levels in patients undergoing CPB at 25°C and 37°C [2]. The temperature protocol in this study was selected to eliminate the potential confounding effect of different perioperative temperatures in the two groups. Similarly, a standardized anesthetic protocol was used in both groups, as several studies have shown a variable effect of different anesthetic and analgesic regimes on the stress response [8, 9, 32–35]. It is likely that the choice of CPB protocol and the anesthetic management had a significant effect on the study findings, and this must be taken into account in future studies.

This study was conducted in a well-defined low-risk patient population with normal cardiac and endocrine function. This ensured homogeneity of the groups, which is essential to avoid various confounding factors in a prospective randomized study. However, as a result of the low-risk nature of the study cohort, there were very few deviations from a routine uncomplicated postoperative course, so that no associations between the magnitude of stress response and clinical outcome could be demonstrated. Further larger studies investigating the possible association between stress hormone levels and clinical outcome or subclinical organ injury markers are required to obtain a clearer picture of the clinical significance of stress response. Our results are in agreement with our previous findings of comparable subclinical renal injury during CPB and OPCAB in a similar patient cohort [14] and may provide an explanation for these findings.

Our data demonstrate that in a low-risk patient population perioperative surgical stress is similar between OPCAB and surgery with CPB. These results cannot be extrapolated to high-risk patients. Patients with poor left ventricular function, unstable symptoms, or other major comorbidities, such as diabetes mellitus or extracardiac arteriopathy, may behave differently and should be investigated separately. Moreover, a similar study in a high-risk population may reveal possible associations between the magnitude of the stress response and clinical outcome.

	Acknowledgments

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
Theodore Velissaris, AFRCS, is supported by the Royal College of Surgeons of Edinburgh and the Wessex Cardiac Trust.

	Discussion

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 
DR SARA J. SHUMWAY (Minneapolis, MN): It might be interesting to measure vasopressin and cortisol release during and after a major vascular case to see whether there was any difference in the levels. Have you looked at a different control group, a noncardiac surgery control group?

DR VELISSARIS: No, we have not looked at that. I suspect there would not be much difference, because in the literature it looks like the main factors of determining stress response are really hemodynamic factors and surgical stimulation. I think that much of the morbidity that has been attributed to conventional cardiopulmonary bypass may not be as we thought previously.

	References

Top Abstract Introduction Patients and methods Results Comment Acknowledgments Discussion References

 

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