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Ann Thorac Surg 2005;80:1751-1757
© 2005 The Society of Thoracic Surgeons

Original article: Cardiovascular

Adverse 30-Day Outcomes After Cardiac Surgery: Predictive Role of Intraoperative Myocardial Acidosis

Dharam J. Kumbhani, MD, SM, Nancy A. Healey, BS, Kunda S. Biswas, MD, Vladimir Birjiniuk, MD, Michael D. Crittenden, MD, Patrick R. Treanor, CCP, Shukri F. Khuri, MD, FACS *

Surgical Service, VA Boston Healthcare System, Harvard Medical School, and Brigham and Women's Hospital, Boston, Massachusetts

Accepted for publication May 11, 2005.

* Address correspondence to Dr Khuri, Surgical Service (112), VA Boston Healthcare System, 1400 V.F.W. Parkway, West Roxbury, MA 02132 (Email: shukri.khuri{at}med.va.gov).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Regional myocardial acidosis in patients undergoing cardiac surgery has been shown to be reflective of regional myocardial ischemia. This study elucidates the relationship between intraoperative regional myocardial acidosis and 30-day postoperative outcomes after cardiac surgery.

METHODS: Intramyocardial tissue pH in the anterior and posterior left ventricular walls was measured in 397 adult patients undergoing valve replacement or coronary revascularization surgery between 1987 and 2001. Dedicated nurses and research assistants prospectively collected preoperative, intraoperative, and outcomes data. Regional myocardial acidosis was defined in terms of pH thresholds identified by recursive partitioning. Adverse 30-day outcome, defined as death or any one of six complications, was the dependent variable in a multivariate logistic regression analysis. A morbidity score was developed on the basis of the sensitivity of each of the six complications in predicting death, and was the dependent variable in a multivariate linear regression analysis.

RESULTS: During the period of aortic clamping, a mean intramyocardial tissue pH less than 6.85 was identified to be significant by recursive partitioning, and was encountered in either the anterior or posterior left ventricular wall in 85.4% of patients. After adjusting for preoperative and intraoperative variables, this pH threshold was found to be significantly associated with increased adverse outcomes within 30 days after surgery (p = 0.045). It was also significantly associated with increase in the morbidity score (p = 0.05).

CONCLUSIONS: Regional myocardial acidosis of a magnitude frequently encountered during aortic clamping is an independent determinant of adverse 30-day outcomes after cardiac surgery. Its reversal by pH-guided myocardial management has the potential of improving postoperative patient outcomes.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

Drs Khuri, Birjiniuk, and Crittenden and Mr Treanor disclose that they have a financial relationship with Terumo.

 

Earlier studies from our institution demonstrated that myocardial tissue pH could be used as a reliable online measure of myocardial tissue ischemia during cardiac surgery [1, 2], allowing the ability to quantify regional myocardial ischemia intraoperatively. These studies resulted in the development of a clinically usable probe that was first used in patients in 1982 [3]. Since then, the probe has undergone many refinements and changes, including incorporation of a temperature thermistor into the design.

Beginning with our early days of measuring myocardial pH in patients, our experience with myocardial pH has evolved through three different phases. During the first phase between 1982 and 1990, we passively monitored and measured the myocardial tissue pH, and observed how the myocardial pH varied as a result of different surgical and reperfusion practices. An observation that became immediately obvious was the wide variation in tissue pH levels between the anterior and posterior walls. Considering normal myocardial pH to be 7.2, a wide variation in the intensity and frequency of acidosis was also observed throughout the course of cardiopulmonary bypass.

The second phase, between 1991 and 1997, consisted of identification of intraoperative maneuvers and techniques to reverse regional ischemic conditions, whereas the third phase, between 1997 and 2001, consisted of specific methods and maneuvers that were specifically aimed at reducing regional myocardial acidosis and ischemia intraoperatively. Collectively, these methods and maneuvers formed the practice of "pH-guided myocardial management" [4].

Between 1982 and 2001, we collected intraoperative myocardial pH information on nearly 700 patients. Systematic analysis of these data demonstrated that regional myocardial acidosis was indeed associated with adverse clinical outcomes in our cohort, including decreased long-term survival [5]. Earlier preliminary analyses using part of the database suggested that regional myocardial acidosis resulted in increased mortality and morbidity within 30 days after surgery [6]. The current study further elucidates this relationship between regional myocardial acidosis and adverse 30-day outcomes after cardiac surgery.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
Patient Population
Between 1982 and 2001, 697 patients underwent intraoperative online monitoring of myocardial tissue pH at the VA Medical Center, West Roxbury, Massachusetts. Complete pH and outcomes data was available for 397 patients, who constituted the study population. Institutional review board approval was obtained, and patient consent forms were used before obtaining U.S. Food and Drug Administration approval for this technology in 1987, after which it was incorporated into our clinical practice.

Myocardial Tissue pH Measurement
Myocardial tissue pH, corrected to 37°C (pH37C), was measured using the Khuri Tissue pH Monitoring System (Vascular Technology, Inc, Lowell, MA) in adult patients undergoing cardiopulmonary bypass, as previously described [3, 7]. Briefly, two right-angled glass microelectrodes were inserted perpendicularly, one into the anterior and one into the posterior left ventricular wall, midway between the apex and the base. They were inserted immediately after beginning bypass, but before applying aortic occlusion, and were removed immediately after the patient was weaned from bypass.

The pH monitoring system continuously measured myocardial tissue pH and temperature. Three pH values were abstracted from this record (Fig 1): pH37C just before aortic clamping, the integrated mean pH37C during the period of aortic clamping, and pH37C at discontinuation of bypass, which was the last value recorded before removal of the probes, after discontinuation of bypass. For each time point in each patient, the lower of the anterior and posterior pH37C values defined the magnitude of regional myocardial acidosis encountered in that patient.



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  		Fig 1. Myocardial tissue pH at 37C (pH37C ) tracings from the anterior (solid line) and posterior (dashed line) left ventricular wall in the course of a three-vessel coronary artery bypass grafting procedure in which the left internal mammary artery was sutured to the left anterior descending coronary artery and two segments of the saphenous vein were sutured to the first and second obtuse marginal artery branches. The aortic clamping (AC) time was 58 minutes, and the total cardiopulmonary bypass (CPB) time was 106 minutes. A total of 1,800 mL of sanguineous cardioplegia was delivered through the aortic root and the proximal ends of the graft. Arrows 1 and 2 in the figure indicate the pH response to the delivery of boluses of blood cardioplegia through the grafts to the first and second obtuse marginal artery branches, respectively. Arrow 3 denotes the response to reestablishment of coronary flow through the left internal mammary artery. The three time points used for data analysis are indicated: before aortic clamping, the integrated mean during the period of aortic clamping, and at the end of cardiopulmonary bypass.

 
Perfusion and Myocardial Management Techniques
Either mild hypothermia (25°C) plus topical cooling with ice slush using conventional bypass circuits (1982 to 1995) or systemic normothermia (32°C) with heparin-bonded bypass circuits (1996 to 2001; Duraflo, Baxter Corp, Irvine, CA) was used. Crystalloid cardioplegia or 4:1 blood cardioplegia was used for coronary artery bypass graft (CABG) procedures. For valve replacement, 4:1 blood cardioplegia was used exclusively since 1991. Dedicated nurses and research assistants prospectively collected preoperative and intraoperative variables on all patients.

Outcomes Data
The clinical outcomes data, prospectively collected by nurse reviewers, was obtained from the database of the Continuous Improvement in Cardiac Surgery Program (CICSP) [8]. Data include the following variables as defined by the CICSP:

Postoperative 30-day mortality defined as death attributable to any cause occurring within 30 days after surgery, or any death occurring after 30 days as a direct result of a perioperative complication from the surgery.
Perioperative myocardial infarction (MI) occurring during surgery or within 30 days after surgery manifested by new Q waves or widening of Q waves by 0.02 seconds on the electrocardiogram.
Low cardiac index defined as a cardiac index less than 2.0 L/min/m2 or peripheral manifestations of low cardiac output (oliguria, hypotension, obtundation) present for more than 6 hours postoperatively requiring inotropic or intraaortic balloon pump support.
Prolonged mechanical ventilation exceeding 48 hours.
Coma defined as significantly decreased level of consciousness for more than 24 hours as evidenced by lack of response to deep, painful stimuli.
Stroke defined as new objective neurologic deficit lasting more than 30 minutes with onset intraoperatively or occurring within 30 days of surgery.
In addition, intraaortic balloon pump use was defined as use of an intraaortic balloon pump anytime after institution of bypass (intraoperatively) or within 48 hours after surgery (postoperatively).
Adverse 30-day outcome was defined as death and any of the above six complications.

Data and Statistical Analysis
Only patients with complete pH and outcomes data were included in the analysis. This resulted in a data set of 397 patients. Missing values for other variables were not imputed. Recursive partitioning of myocardial pH37C values before aortic clamping, during the period of aortic clamping, and at the end of reperfusion was performed in an attempt to identify the best threshold of myocardial pH that was most significantly associated with the outcome. Failure to identify a threshold indicated a lack of relationship between the variable and the outcome [9]. From this recursive partitioning, myocardial acidosis was defined as pH37C below the identified threshold, a dichotomous variable. Age, body surface area, preoperative ejection fraction, preoperative serum creatinine, duration of aortic clamping and bypass, and total volume of cardioplegia solution used were treated as continuous variables. Year of study (1987 to 1990, 1991 to 1997, 1997 to 2001), type of surgery (CABG, valve only, valve + CABG, redo surgery), and surgeon (three) were treated as categorical variables. For these variables, the category with the lowest adverse outcomes rates was chosen as the reference category in the logistic regression model. All others were treated as binary variables. The likelihood ratio test, using PROC LOGISTIC in SAS, was used to compare the univariate predictors of 30-day mortality. Multivariate logistic regression models were constructed, with adverse 30-day outcome as the dependent variable. On the basis of Hosmer-Lemeshow guidelines, only those variables with p < 0.2 in the univariate analysis were entered into a forward stepwise procedure [10]. Two-way interactions of important risk factors were examined for statistical significance. The c statistic, which is analogous to the area under the receiver-operating characteristic curve [11], was calculated to estimate the discriminative value of the predictive models. Calibration of the model was tested by the Hosmer-Lemeshow test statistic for goodness-of-fit [12].

A sensitivity analysis determined the sensitivity of each of the six complications in predicting death. On the basis of this analysis, integer scores were assigned to each complication [13]. As this score was not normally distributed, a log-transformed morbidity score was constructed such that morbidity score = ln (sensitivity score + 1), where ln indicates the natural logarithm. This was then entered as the dependent variable in a multivariate linear regression analysis.

Statistical analyses were performed using SAS version 8.2 (SAS Institute, Cary, NC). All p values were two-tailed, with statistical significance set at 0.05. All confidence intervals were calculated at the 95% level.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
The operations performed consisted of primary surgery or reoperation for (1) CABG using saphenous vein or internal mammary artery, (2) aortic valve replacement with concomitant mitral valve replacement, or (3) CABG with valve repair or replacement (aortic valve replacement or mitral valve replacement). The distribution of preoperative, demographic, and intraoperative variables in patients having any 30-day adverse event compared with those with no 30-day adverse event is shown in Table 1. The mean number of grafts per patient was 2.1 ± 1.2. (range, 0 to 5).


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  		Table 1. Baseline Characteristics of Study Population (n = 397) a
 
Altogether, 96 (24.2%) of the 397 patients in our study population had an adverse postoperative outcome within 30 days. The most frequently occurring complications were mechanical ventilation greater than 48 hours (observed in 43 patients [10.8%]), intraaortic balloon pump use (32 patients [8.1%]), and low cardiac output (20 patients [5.0%]). Postoperative mortality was observed in 18 patients (4.5%).

Table 2 shows the results of recursive partitioning. Threshold values that related to adverse 30-day outcomes were identified for myocardial pH37C before aortic clamping (6.35) and during the period of aortic clamping (6.85). None were identified for myocardial pH37C during reperfusion. On the basis of these thresholds, myocardial acidosis was observed in 43 patients (13.2%) before aortic clamping and in 339 patients (85.4%) during the period of aortic clamping. Patients with myocardial acidosis before and during the period of aortic clamping were more likely to develop complications postoperatively, as compared with patients who did not have acidosis. A comparison of complication rates between patients with pH37C less than 6.85 during aortic clamping and those with pH37C of 6.85 or greater during the period of aortic clamping is shown in Figure 2. In general, complications were more common in the group with myocardial acidosis, although only the composite end point was statistically significant.


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  		Table 2. Myocardial pH37C Thresholds Significantly Affecting 30-Day Adverse Outcomes
 


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  		Fig 2. Comparison of frequency rates of 30-day postoperative outcomes in patients who sustained regional myocardial acidosis (gray bars; pH37C < 6.85) during aortic clamping compared with those who did not (black bars; pH37C ≥ 6.85). (CPB = cardiopulmonary bypass; CPR = cardiopulmonary resuscitation; IABP = intraaortic balloon pump; MI = myocardial infarction.)

 
Patients experiencing an adverse outcome within 30 days after surgery were more likely to be female, have a New York Heart Association class of III or IV, be a current smoker, be operated on during the earlier years of the study, undergo reoperation, undergo combined CABG and valve surgery, have longer durations of aortic clamping and bypass, receive a larger volume of cardioplegia solution during surgery, and, as mentioned earlier, have myocardial acidosis both before and during the period of aortic clamping (Table 1).

The multivariate analysis revealed that the independent significant predictors of adverse outcomes were female sex, surgery during earlier years of the study, longer duration of bypass, and mean pH37C less than 6.85 during aortic clamping (Table 3). After adjusting for other variables in the model, acidosis during the period of aortic clamping was associated with a nearly threefold increase in the risk of developing an adverse postoperative outcome within 30 days (relative risk, 2.84; 95% confidence interval, 1.02 to 7.89; p = 0.045). The c index for this model was 0.76 and the Hosmer-Lemeshow test gave a p value of 0.08 ({chi}2 = 13.9 with 8 degrees of freedom), indicating that the model was fitting the data well.


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  		Table 3. Multivariate Models Depicting Predictors of Adverse 30-Day Outcomes and Morbidity Score
 
All complications, other than stroke, were associated with an increased risk of postoperative mortality. Presence of any one of the six postoperative complications increased the risk of postoperative mortality by about 10 times (relative risk, 9.75; 95% confidence interval, 3.53 to 26.94; p < 0.0001).

The results of the sensitivity analysis leading to the morbidity score are demonstrated in Table 4. Of the six complications, low cardiac output had the highest sensitivity in predicting mortality, with 7 of the 20 patients who exhibited low cardiac output dying within 30 days of surgery (39% mortality). Stroke was the least sensitive, with only 1 death (6% mortality). The sensitivity-based score ranged from 0 to 146. The morbidity score, which was generated by log-transformation, ranged from 0 to 4.98. The highest morbidity score observed in our patient population was 4.82, corresponding to a sensitivity score of 123. The mean scores for those with and those without myocardial acidosis were 0.77 and 0.40, respectively (p = 0.039). Thus, myocardial acidosis was associated with a 0.37 unit, or 92.5%, increase in the severity of the morbidity score. We compared the sensitivity scores generated in our study population with a different population of cardiac surgery patients operated on during a comparable period of time, using data from the CICSP database. The results were similar (data not shown).


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  		Table 4. Sensitivity Analysis and Morbidity Score
 
The results of the multivariate linear regression analysis, with morbidity score as the outcome variable, are shown in Table 3. These results are very similar to those of the logistic regression analysis. Diabetes, longer bypass time, and myocardial acidosis during the period of aortic clamping were identified as significant independent predictors of the morbidity score. This model had an adjusted R 2 value of 0.23.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
This study, which was conducted in 397 patients undergoing cardiac surgery, shows that during the period of aortic clamping, a myocardial tissue pH37C of 6.85 defines an acidosis threshold below which the risk of 30-day postoperative outcomes is significantly increased. This pH37C threshold was associated with a nearly threefold increase in the risk of adverse postoperatively outcomes, and about a twofold increase in the severity of the patients' morbidity score.

For the purpose of this study, we elected to study a composite well-defined group of outcomes together because the small sample size did not provide enough power to study them separately. Hammermeister and colleagues [14], also using the CICSP database, have used a similar composite end point, even though they studied a patient population that exceeded 10,000 veterans. Our findings are similar to theirs; for example, they reported a 15% complication rate in CABG patients, whereas we found this rate to be 15.4% in our study. They also found mechanical ventilation longer than 48 hours to be the most common postoperative complication, with an incidence of 7.8%, compared with 10.9% in our study. The preoperative univariate predictors of adverse 30-day outcomes were similar in both studies too. In the multivariate model, the predictive role of myocardial acidosis was unique to our study, as myocardial pH37C measurements were only obtained in our institution. Predictive factors other than pH37C that were identified in the multivariate analyses in our study have been shown to be independent predictors of adverse short-term postoperative outcomes by various other studies as well [15–24].

The relationship between regional myocardial acidosis and regional myocardial ischemia has been well established at our institution. Myocardial tissue pH, measured with the technology used in this study, has been shown to be reflective of regional myocardial tissue carbon dioxide partial pressure measured with mass spectrometry [2]. Under ischemic conditions, the respective measurements of regional myocardial tissue pH and carbon dioxide partial pressure have been shown to correlate with each other [2], and with adjacent intramural ST-segment changes [25], regional myocardial blood flow [26], qualitative ultrastructural ischemic changes [1, 26], and intracellular pH and intracellular high-energy phosphates [27]. The evolution of these findings, in the context of clinical intraoperative monitoring of myocardial pH, led to the genesis of pH-guided myocardial management, which is directed at reducing or totally ameliorating intraoperative regional myocardial acidosis [4, 27, 28]. The demonstration, in this study, that pH37C during the period of aortic clamping, was most significant in determining 30-day adverse outcomes is promising, because most techniques of pH-guided myocardial management have been directed at reducing acidosis during this period of global ischemia. For example, these techniques allow targeted delivery of the cardioplegia solution to acidotic or ischemic segments of the myocardium, thus affecting a more efficient washout of accumulated tissue hydrogen ions and a more homogeneous distribution of the substrate to the left ventricular wall [4].

In an earlier study [29], we found that there was a very strong correlation between pH values at different periods, such that pH values at each time point are dependent on pH values preceding it. Avoiding acidosis during aortic occlusion decreased the risk of developing acidosis during reperfusion by 50%. This further highlights the importance of avoiding regional myocardial acidosis throughout the course of the surgery.

Previous studies have claimed that acidosis was protective to the myocardium during ischemia [30, 31]. However, the value of acidosis shown to be protective in these studies was around 7.0. During the 14-year period of this study, before conducting the present analysis, we had observed clinically that the patients who had the best outcomes were those in whom the pH during the period of aortic clamping had been kept at approximately 6.80. The present analysis supported this clinical observation, and established the adversity of a mean pH37C below 6.85 during the period of aortic clamping. We have also earlier demonstrated that pH37C values less than 6.80 trigger the apoptotic cascade in myocardial cells [32]. This was found to be proportional to the severity and duration of acidosis. It has also been well established in physiology that a pH of 6.8 is optimal for intracellular enzymatic function. Hence, we believe that our identified threshold of 6.85 in this paper has both biologic and translational relevance and is not merely a statistical threshold chosen to demonstrate significance.

Using recursive partitioning, we had previously identified pH37C less than 6.34 during aortic clamping and pH37C less than 6.73 at the end of cardiopulmonary bypass as threshold values most significantly associated with long-term survival [5]. This indicates that compared with adverse 30-day outcomes, a greater degree of acidosis is required to influence long-term survival. This could again be related to the fact that severe acidosis results in an escalation of the apoptotic cascade in myocytes (as mentioned above) [32], which can potentially result in congestive cardiac failure and thus influence long-term survival.

The main limitation of this study is the fact that it has emanated from a single institution and that any validation of the findings will require prospective multicenter studies. One such study, involving centers in Europe and the United States, is currently underway. Another concern is the use of recursive partitioning to identify a threshold pH value most significantly associated with adverse outcomes. Recursive partitioning is often used in exploratory analyses to identify the best threshold of a continuous variable that is significantly associated with the outcome [9]. Inasmuch as, to date, pH monitoring and management has been studied only at our institution, one of our endeavors was to provide the surgeon with a threshold or a guideline below which outcomes were adversely affected. This was the reason that we elected to dichotomize the pH values. In light of the marginal statistical significance reported in this manuscript (p = 0.047), these values might be perhaps viewed as trends. However, they do provide enough information to guide the new practice of pH-guided myocardial management until such time that multicenter studies can be performed and these thresholds are either verified or modified.

In conclusion, regional myocardial acidosis of a magnitude frequently encountered during aortic clamping is an independent determinant of adverse 30-day outcomes after cardiac surgery. The application of pH-guided myocardial management techniques that would prevent myocardial tissue pH from falling below 6.85 during the period of aortic clamping is likely to improve 30-day patient outcomes after cardiac surgery.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This work was supported by the Richard Warren Surgical Research and Educational Fund, Westwood, MA.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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Right arrow Myocardial protection

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