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Anesth Analg 2004;99:1024-1031
© 2004 International Anesthesia Research Society
doi: 10.1213/01.ANE.0000132543.65095.2C

CARDIOVASCULAR ANESTHESIA

A Comparison Among Portal Lactate, Intramucosal Sigmoid pH, and {Delta}CO2 (PaCO2 – Regional PCO2) as Indices of Complications in Patients Undergoing Abdominal Aortic Aneurysm Surgery

Abele Donati, MD*, Oriana Cornacchini, MD*, Silvia Loggi, MD*, Sandro Caporelli, MD*, Giovanna Conti, MD*, Stefano Falcetta, MD*, Francesco Alò, MD{dagger}, Gabriele Pagliariccio, MD{dagger}, Elisabetta Bruni, MD*, Jean-Charles Preiser, MD PhD{ddagger}, and Paolo Pelaia, MD*

*Department of Neuroscience, Anesthesia and Intensive Care Unit, and {dagger}Department of Vascular Surgery, Marche Polytechnique University, Ancona, Italy; and {ddagger}Department of Intensive Care, University Hospital of Liege, Liege, Belgium

Address correspondence and reprint requests to Abele Donati, MD, Rianimazione Clinica, Ospedale Regionale Torrette, Via Conca 1, 60020 Torrette, Ancona, Italy. Address e-mail to donati{at}indi.it


   Abstract
Top
 Abstract
Introduction
 Methods
 Results
 Discussion
 References
 
Our aim in this observational, prospective, noncontrolled study was to detect, in 29 patients who underwent abdominal aortic aneurysm (AAA) surgery, correlations between the incidence of postoperative organ failure and intraoperative changes in arterial and portal blood lactate; changes in intramucosal sigmoid pH (pHi); differences between sigmoid PCO2 and arterial PCO2 ({Delta}CO2); and hemoglobin (Hb). Hb, arterial blood lactate concentrations, pHi, and {Delta}CO2 (air tonometry) were recorded at the start of anesthesia (T0), before aorta clamping (T1), 30 minutes after clamping (T2), and at the end of surgery (T3). Portal venous lactate concentrations were recorded at T1 and T2. Patients were stratified into two groups: group A patients had no postoperative organ failure, and group B patients had one or more organ failures. As compared with group A (n = 16), group B patients (n = 13) had a lower pHi value at T2 and T3 and a higher {Delta}CO2 at T3. A pHi value of <7.15 was a predictor of organ failure, with a sensitivity of 92.3%, a specificity of 68.8%, and positive and negative predictive values of 70.6% and 91.7%, respectively, whereas a {Delta}CO2 value of >28 mm Hg predicted later organ failure with a sensitivity of 92.3%, a specificity of 62.5%, and positive and negative predictive values of 66.6% and 90.9%, respectively. Portal venous lactate concentrations were larger in group B at T2 (P < 0.001), and an increase ≥5 g/dL predicted later postoperative organ failure with a sensitivity of 92.3%, a specificity of 100%, and positive and negative predictive values of 100% and 94.1%, respectively. The comparison of the receiving operator characteristic curves to test the discrimination of each variable and the logistic regression analysis revealed that the increase in portal lactate was the best predictor for the development of postoperative organ failure. Hb concentration was significantly smaller in group B at T0 (13.8 ± 1.0 g/dL versus 12.2 ± 2.2 g/dL) and T2 (10.9 ± 1.2 g/dL versus 9.1 ± 1.9 g/dL). In conclusion, both pHi and {Delta}CO2 are reasonably sensitive prognostic indices of organ failures after AAA surgery, but they are less specific and accurate than portal venous lactate.

IMPLICATIONS: Although older studies cannot correlate with outcome, this study is the first comparison of the values of three indirect markers of gut ischemia—portal venous lactate concentration, intramucosal intestinal pH, and gradient between regional and arterial PCO2—as predictors of organ failure after surgery for abdominal aortic aneurysm.


   Introduction
Top
 Abstract
 Introduction
Methods
 Results
 Discussion
 References
 
Gut hypoxia is a phenomenon that occurs during major abdominal operations (1,2). During surgical repair of abdominal aortic aneurysms (AAA) (3), gut hypoxia often occurs as a consequence of clamping of the aorta, reduced intraoperative arterial blood pressure, activation of the inflammatory cascade, or effects of anesthetics. Importantly, the presence of gut hypoxia is associated with an increased incidence of postoperative complications (4), including multiple organ dysfunction syndrome. Therefore, early detection of gut hypoxia is important to optimize therapeutic management.

However, diagnosis and assessment of the severity of gut hypoxia are challenging. Inadequate splanchnic perfusion can be indirectly detected by several approaches, including increased concentrations of portal venous lactate and a widened portal venous/arterial lactate gradient (5–8). Intestinal tonometry is another technique of clinical monitoring of intestinal perfusion: it can detect early mucosal ischemia, reflected by a decrease in intramucosal intestinal pH (pHi) or a widening of the gradient between regional and arterial PCO2 ({Delta}CO2) (9). Both pHi and {Delta}CO2 were validated as reliable prognostic indices for the development of organ failure after major surgery (10). The aim of this study was to compare the values of portal venous lactate, sigmoidal pHi, and {Delta}CO2 as early indicators of postoperative organ failure after AAA surgery.


   Methods
Top
 Abstract
 Introduction
 Methods
Results
 Discussion
 References
 
This observational, prospective, open-labeled noncontrolled study was approved by the Hospital Ethical Committee, and informed consent was obtained from the patients before surgery. A cohort of 29 consecutive patients undergoing elective transperitoneal surgery for AAA was enrolled in the study. Twenty-six patients were male and 3 were female, with a mean age of 73.0 ± 6.9 yr.

A post hoc stratification of the patients in both groups was planned according to the absence (group A) or the presence (group B) of one or more postoperative organ failures, defined as shown in Table 1 (11). The observation period lasted until patient discharge from the hospital. Clinicians managing the patients postoperatively were not aware of the tonometric and lactate values.


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  		Table 1. Definition of Organ Failure, Modified (11)
 
All patients were treated before surgery with H2-blockers (ranitidine 300 mg per os) and premedicated with diazepam (0.1 mg/kg). No patient had an epidural catheter placed. Anesthesia was induced with fentanyl (0.01 mg/kg) and sodium thiopental (4 mg/kg), and muscle relaxation was induced with vecuronium (0.08 mg/kg). After orotracheal intubation, anesthesia was maintained with sevoflurane, nitrous oxide, vecuronium, and fentanyl; fraction of inspired oxygen was maintained at 0.40. Intraoperative monitoring included 1) on-line electrocardiogram, 2) pulse oximetry, 3) continuous arterial blood pressure, 4) monitoring of blood gas variables, 5) sigmoid tonometry, 6) urinary output, and 7) hemoglobin (Hb) concentration. Transfusion of packed red cells was considered for Hb levels less than 8 g/dL, and no patient received any red cell transfusion before surgery. Dobutamine infusion was started when cardiac failure was suspected (hypotension with mean arterial blood pressure less than 70 mm Hg not responsive to fluid challenge; oliguria with urine output less than 0.5 mL · kg– · h–1). All the patients were tracheally extubated during the first postoperative hour.

Blood gas analysis was performed with the automatic analyzer RapidLab 865 Chiron Diagnostic (Bayer, Leverkusen, Germany), and values were corrected for blood temperature. Hb concentration was measured by using the same instrument.

Measurement of lactate levels in systemic arterial and portal circulation was performed with a Vitros 950 Chemistri System analyzer. This system is based on an enzymatic technique that determines by spectroscopy the color changes due to the presence of a lactate-activated chromogenic substrate. Systemic lactate determinations were performed at the time of anesthesia induction (T0), before clamping (T1), 30 min after clamping (T2), and at the end of surgery (T3). Portal venous lactate determinations were performed at T1 and T2 through a sample of portal venous blood taken by the surgeon, and the difference in portal venous lactate concentration (T2 – T1; {Delta} portal venous lactates) was calculated.

A TRIP tonometer (Tonometrics Division, Instrumental Corp., Helsinki, Finland) was used to measure regional CO2 (PrCO2) after automatic calibration of the instrument. This tonometer is based on principles and techniques described elsewhere (12,13). The tonometer is a silicon 8F catheter with a balloon tip and a semipermeable membrane that allows diffusion of gas, but not fluids. A tonometer is introduced intrarectally, positioned in the sigmoid colon, and connected to the Tonocap (Datex, Helsinki, Finland) device to perform air tonometry. The surgeon manually checked the positioning of the tonometer during the intervention. The tonometer was maintained in situ throughout the operation and was removed after tracheal extubation. PaCO2 was measured at T0, T1, T2, and T3. At the same time, pH was recorded and an arterial blood sample was taken to measure PaCO2 and [H+], used for the calculation of {Delta}CO2 (PrCO2 – PaCO2).

Outcome was defined as the absence or presence of one or more postoperative organ failures. At each time point, the means and standard deviations of heart rate, mean arterial blood pressure, PaO2/fraction of inspired oxygen ratio, PaCO2, pHi, {Delta}CO2, systemic and portal venous lactates, and Hb were calculated for both groups of patients. Gaussian distribution was also verified with the Kolmogorov-Smirnov test. Continuous variable measurements expressed as means were compared by using two-way analysis of variance, with Student’s t-test or Student’s t-test with Welch’s correction if variances were significantly different and with Bonferroni’s correction for multiple comparisons when appropriate. Sensitivity, specificity, and positive and negative predictive values to predict postoperative complications were calculated for pHi, {Delta}CO2, and {Delta} portal venous lactates. Fisher’s exact test was used to test significance, and power was calculated for each analysis.

All P values are two sided, and a threshold {alpha} of 0.05 was used to assign significance (GraphPad 2.0; GraphPad Inc., San Diego, CA). The area under the receiving operator characteristic curve (ROC) was calculated to detect the discrimination ability of the variables for complications (SPSS 10.1; SPSS Inc., Chicago, IL). Finally, logistic regression was performed to detect which variables had an independent significant value to predict outcome (SPSS 10.1).


   Results
Top
 Abstract
 Introduction
 Methods
 Results
Discussion
 References
 
Of the 29 patients enrolled in this study, 16 were classified in group A, and 13 qualified for group B, because these experienced at least 1 postoperative new organ failure (Table 1). Six patients developed acute renal failure, three developed heart failure, three had hepatic failure, and one had a multiorgan failure and eventually died. Infrarenal aortic clamping was used in all patients.

There was no difference between groups in age, number of preoperative morbidities, aortic clamping time, and type of bypass performed (aortoaortic or aortoiliac). Patients without complications were discharged from the hospital significantly earlier than patients with complications (Table 2).


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  		Table 2. Clinical Features, Surgical Notes, and Length of Postoperative Stay in the Hospital Within Each Group
 
Arterial lactate concentrations increased significantly from T0 to T3 in group A (P < 0.01) and from T0 to T2 and T3 (P < 0.01 and P < 0.001, respectively) in group B (Table 3). The trend of systemic arterial lactate levels wassimilar in the two groups.


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  		Table 3. Trends of Each Variable in the Two Groups (Mean ± SD)
 

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  		Table 3. Continued
 
The {Delta} portal venous lactates significantly increased in group B (P < 0.001) but not in group A (Fig. 1). The difference between groups was significant at T2 (P < 0.001). With a cutoff value for {Delta} portal venous lactates at 5 mg/dL, 12 of the 13 patients in group B and none of the patients in group A had values equal to or more than 5 mg/dL. The sensitivity to predict postoperative organ failure was 92.3%, and the specificity was 100% (P < 0.001; power, 99%). The positive and negative predictive values were 100% and 94.1%, respectively. The area under the ROC was 0.971 (SE, 0.031; 95% confidence interval [CI], 0.911–1.031; P < 0.001 versus the null hypothesis area = 0.5) (Fig. 2).


Figure 1
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  		Figure 1. Portal venous lactate concentrations at different times in the two groups. Time T1 is before clamping; T2 is 30 min after clamping. Columns indicate mean and SD at each time of each group. #P < 0.001 versus T1 in group B; *P < 0.001, group A versus group B at T2.

 

Figure 2
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  		Figure 2. Area under the receiver operating characteristic curves of intramucosal sigmoid pH (pHi), gradient between regional and arterial PCO2 ({Delta}CO2), and {Delta} portal venous lactates.

 
The pHi decreased in both groups during surgery (Table 3). Overall, the decrease was larger in group B than in group A (P < 0.01). As compared with the value recorded at the same time point, the decrease from T0 was larger in group B than in group A for T2 (P < 0.05) and T3 (P < 0.01). The mean of the lowest values (the lowest pHi value at any of the observation points of each patient) was significantly lower in group B than in group A (6.99 ± 0.15 versus 7.15 ± 0.17; P < 0.05). A lowest pHi value less than 7.15 predicted the occurrence of organ failure with a sensitivity of 92.3% and a specificity of 68.8% (P < 0.01; power, 91%) (Fig. 3, top). The positive and negative predictive values were 70.6% and 91.7%, respectively. The area under the ROC was 0.755 (SE, 0.096; 95% CI, 0.567–0.943; P = 0.020) (Fig. 2).


Figure 3
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  		Figure 3. (Upper panel) The lowest intramucosal sigmoid pH (pHi) value at any of the observation points of each patient of the two groups. With pHi 7.15 as the cutoff, there was 92.3% sensitivity and 68.8% specificity to predict complications and a positive and negative predictive value of 70.6% and 91.7%, respectively (power = 91%). Columns indicate mean and SD at each time of each group. (Lower panel) The highest gradient between regional and arterial PCO2 ({Delta}CO2) value at any of the observation points of each patient of the two groups. With a {Delta}CO2 of 28 mm Hg as the cutoff, there was 92.3% sensitivity and 62.5% specificity to predict complications and a positive and negative predictive value of 66.6% and 90.0%, respectively (power = 82%). Columns indicate mean and SD at each time of each group.

 
There was a significant increase of {Delta}CO2 over time within each group (Table 3), although it was larger in group B than in group A (P < 0.01). {Delta}CO2 was significantly larger in group B than in group A at T2 and T3 (P < 0.05). The mean peak {Delta}CO2 (the highest CO2 value at any of the observation points of each patient) was significantly lower in group A (32.9 ± 24.2 mm Hg) than in group B (53.9 ± 28.4 mm Hg; P < 0.05). With a cutoff level of 28 mm Hg {Delta}CO2, sensitivity was 92.3% and specificity was 62.5% (P < 0.01; power, 82%) (Fig. 3, bottom). Positive and negative predictive values were 66.6% and 90.9%, respectively. The area under the ROC was 0.740 (SE, 0.094; 95% CI, 0.556–0.925; P = 0.028) (Fig. 2).

The other differences between the patients from group A and those from group B included Hb values, intraoperative blood loss, and number of transfusions. Blood loss was larger in group B than in group A (1119 ± 645 mL versus 647 ± 462 mL; P < 0.05). The area under the ROC was 0.692 (SE, 0.104; 95% CI, 0.489–0.895; P = 0.079). Accordingly, Hb progressively decreased from T0 to T1 in group B (P < 0.05), from T0 to T2 in both groups (P < 0.001), and from T0 to T3 in both groups (P < 0.01 in group A and P < 0.05 in group B). The average values of Hb at T0 and T2 were significantly less in group B than in group A (Table 3). The number of packed red cells transfused was still more in group B than in group A (1.5 U [range, 0–3 U] versus 0.4 U [range, 0–3 U]; P < 0.05). The area under the ROC was 0.702 (SE, 0.103; 95% CI, 0.501–0.903; P = 0.066). No other blood products were transfused during the operation. The area under the ROC for the Hb values at T0 as a predictor of complications was 0.755 (SE, 0.091; 95% CI, 0.577–0.932; P = 0.020). No other significant difference was found in the other variables (Table 3).

Comparing the differences between areas of the 3 ROC curves (Fig. 2), {Delta} portal venous lactates was significantly more powerful than pHi (difference between areas, 0.216; SE, 0.086; 95% CI, 0.047–0.386; P = 0.012) and {Delta}CO2 (difference between areas, 0.231; SE, 0.092; 95% CI, 0.051–0.410; P = 0.012). No differences were found between pHi and {Delta}CO2 ROC curves (difference between areas, 0.015; SE, 0.049; 95% CI, –0.082 to 0.111; P = 0.770) to predict postoperative organ failure.

The {Delta} portal venous lactates ROC curve was also more powerful than Hb at T0 (difference between areas, 0.216; SE, 0.089; 95% CI, 0.042–0.391; P = 0.015), the number of transfused packed red cells (difference between areas, 0.269; SE, 0.097; 95% CI, 0.079–0.460; P = 0.006), and blood loss (difference between areas, 0.279; SE, 0.098; 95% CI, 0.087–0.470; P = 0.004). The ROC curves for pHi, {Delta}CO2, Hb at T0, number of transfused packed red cells, and blood loss did not differ. The logistic regression revealed that the independent predictors of postoperative organ failure included {Delta} portal venous lactates (odds ratio, 3.513; P = 0.029), Hb at T0 (odds ratio, 0.498; P = 0.045), and {Delta}CO2 (odds ratio, 1.490; P = 0.049).


   Discussion
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
References
 
In this study, we compared three indices of gut hypoxia recorded during surgery and found that the changes in each of these three variables were sensitive predictors for the development of later organ failures. However, the portal venous lactate gradient was a more accurate and more specific predictor of postoperative organ failure than pHi or {Delta}CO2, as indicated by the sensitivity and specificity, the positive and negative predictive values, the comparison of the ROC curves, and the logistic regression.

The findings of this study strongly support the role of gut hypoxia in the pathogenesis of multiple organ dysfunction after AAA surgical repair. The association between low Hb and an increased incidence of organ failure suggests that gut hypoxia is amplified by preoperative and postoperative anemia. The balance between the benefit of blood transfusions on gut perfusion and the potential deleterious effects (14) can hardly be deducted from the data recorded in this study, although the differences in the amount of blood transfusions could represent a risk factor per se for the development of organ failure and could therefore be a confounding factor for the interpretation of the results. However, there are other studies that suggest that patients with a lower level of hematocrit are affected by more complications, such as myocardial ischemia (15,16). In any case, patients with complications had lower Hb levels before surgery, and intraoperative transfusion did not reverse this association.

The ischemia/reperfusion phenomenon can be advocated to explain our findings. Indeed, ischemia/reperfusion occurs during clamping and declamping of the abdominal aorta (17,18) and can trigger the absorption of bacteria or bacterial endotoxins across the ischemic intestinal wall and the release of cytokines from the intestine. These cytokines, also through vascular endothelial damage, may play a significant role in the pathogenesis of organ dysfunction (17,19). In this study, we did not record the microbiological or immunological data that could confirm such a mechanism. However, we (2) and others (1) previously observed increased levels of proinflammatory cytokines during abdominal and AAA surgery in patients who developed postoperative complications.

The reasons for the better specificity of the lactate gradient than the tonometric variables may be related to the fact that portal lactate is released by the full thickness of the intestinal wall in case of hypoxia, whereas the variables recorded by tonometry reflect only mucosal perfusion. In addition, the absence of severe hepatic failure at the time of surgery suggests that the portal lactate is appropriately cleared by the liver, as illustrated by the poor sensitivity of arterial lactate concentrations as an index of gut hypoxia and predictor of postoperative organ failure (20,21). Very importantly, there was no organ failure in patients with a portal venous lactate gradient less than 5 mg/dL. In some patients without an increase in portal lactate gradient or any organ failure, a preexisting thrombosis of the inferior mesenteric artery could be present (22), and therefore gut perfusion is not affected by infrarenal aortic clamping.

The positive predictive values of pHi and {Delta}CO2 recorded by tonometry were reasonably high and consistent with those in previous reports. There was a tendency for lower pHi and higher {Delta}CO2 from the beginning of anesthesia, and this was consistent with Poeze et al. (23), who demonstrated that patients with lower preoperative pHi have a worse outcome than patients with normal pHi. In both groups, there was a significant reduction of pHi and increase of {Delta}CO2. During anesthesia, a decrease in global hemodynamic indices is normal (24), and oxygen debt is common during anesthesia (25). The degree of this debt determines postoperative complications and death (25,26). The major advantage of this noninvasive technique of monitoring the gut mucosal perfusion is the early detection of an ischemic intestinal lesion before the occurrence of clinically detectable symptoms and signs (27). Another major advantage over portal lactate determination is the possibility of postoperative monitoring that was assessed and validated by others (13). Indeed, previous studies have shown that a sigmoid pHi less than 7.1 for more than two hours is associated with large concentrations of endotoxins and cytokines (28) and is predictive of major complications and death. In a study by Björck and Lindberg (29), the severity of the mucosal ischemic lesions classified by colonoscopy was correlated with the values of sigmoid pHi monitoring with a sensitivity of 90% and a specificity of 100%.

Other groups have tested the diagnostic accuracy of sigmoid pHi in the evaluation of colon ischemia in patients undergoing AAA surgery (30,31). Sigmoid pHi was related to the severity of colonic damage andthe duration of ischemia (30,31). In this study, the level of sigmoid pHi that appears able to discriminate patients with complications is 7.15, and most (12 of 13) patients with complications showed sigmoid pHi levels less than the cutoff. Most levels (11 of 16) were more than the cutoff in patients without complications. In our study, we showed that pHi decreases before aortic clamping, but the lowest values were shown 30 minutes from clamping and at the end of surgery. This is consistent with published results by other groups indicating that the lowest levels of sigmoid pHi were found between four and six hours after aortic clamping (12). In this study, sigmoid pHi monitoring was performed only at the end of surgery and not during postoperative evaluation. A good correlation between direct and tonometer-obtained measurement of pHi has been reported by other groups as well (22).

Work by Heino and Hartikainen (32) confirmed the sensitivity of {Delta}CO2 in identifying regional splanchnic hypoperfusion, as previously suggested by Schlichtig and Boweles (33). In our study, calculation of the difference between PrCO2 and PaCO2 was not only a sensitive marker, but also an independent predictor of organ failure. Differences in surgical techniques and the presence of collateral circulation between the superior and inferior mesenteric arteries were not accounted for in this study. The possible presence of collateral circulation supports our hypothesis that patients with significant anastomosis between splanchnic and systemic circulation may display lower degrees of colon ischemia with higher sigmoid pHi levels and lower portal venous lactates. In all patients with complications, the difference between PrCO2 and PaCO2 was increased before, during, and after clamping, as shown previously by Schlichtig and Boweles (33).

In conclusion, although the pathogenesis of the reduced pHi is still controversial, the results of this pilot study indicate that pHi and {Delta}CO2 are sensitive prognostic indices during AAA surgery and therefore suggest that tonometry may identify patients at higher risk of organ failure in the postoperative period. The {Delta} portal venous lactates are more specific then tonometric variables, and this study confirms experimental studies that indicate portal venous lactate as an important index of gut hypoperfusion. Further studies with a large number of patients need to prospectively validate our cutoff points for pHi and {Delta}CO2. New therapeutic strategies, such as fenoldopam infusion (a dopamine D1-like receptor agonist) during surgery, could be tested in a prospective study to treat splanchnic ischemia by applying the cutoff points (pHi <7.15 and {Delta}CO2 >28 mm Hg) that were used in our study.


   References
Top
 Abstract
 Introduction
 Methods
 Results
 Discussion
 References
 

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Accepted for publication April 27, 2004.




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Lippincott, Williams & Wilkins Anesthesia & Analgesia® is published for the International Anesthesia Research Society® by Lippincott Williams & Wilkins with the assistance of Stanford University Libraries' HighWire Press®. Copyright 2006 by the International Anesthesia Research Society. Online ISSN: 1526-7598   Print ISSN: 0003-2999 HighWire Press