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J Appl Physiol 82: 558-562, 1997;
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Journal of Applied Physiology
Vol. 82, No. 2, pp. 558-562, February 1997
SYSTEMIC CIRCULATION AND FLUID BALANCE

Esophageal PCO2 as a monitor of perfusion failure during hemorrhagic shock

Yoji Sato1, Max Harry Weil1,2, Wanchun Tang1,2, Shijie Sun1,2, Jianlin Xie1, Joe Bisera1,2, and Hidehiro Hosaka3

1 The Institute of Critical Care Medicine, Palm Springs 92262-5309; 2 The University of Southern California School of Medicine, Los Angeles, California 90033-1039; and 3 Nihon Kohden Corporation, Tokyo 161, Japan

ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES

ABSTRACT

Sato, Yoji, Max Harry Weil, Wanchun Tang, Shijie Sun, Jianlin Xie, Joe Bisera, and Hidehiro Hosaka. Esophageal PCO2 as a monitor of perfusion failure during hemorrhagic shock. J. Appl. Physiol. 82(2): 558-562, 1997.---Measurement of gastric wall PCO2 (PgCO2) by tonometric method has emerged as an attractive option for estimating visceral perfusion during circulatory shock. However, gastric acid secretion obfuscates the tonometric measurement. We, therefore, investigated the option of measuring PCO2 in the esophagus to minimize these restraints. Hemorrhagic shock was induced in five Sprague-Dawley rats, and five rats served as sham controls. PgCO2 was measured with an ion-sensitive field effect transistor that was surgically implanted into the gastric wall. Esophageal luminal PCO2 (PeCO2) was measured by a second ion-sensitive field effect transistor sensor. During hemorrhagic shock, mean aortic pressure declined from 150 to 50 mmHg. Gastric blood flow decreased from 58 to 12 ml · min-1 · 100 g-1 (21% of preshock) and esophageal blood flow from 44 to 7 ml · min-1 · 100 g-1 (16% of preshock). PgCO2 simultaneously increased from 47 to 116 Torr and PeCO2 from 47 to 127 Torr. The increases in PgCO2 were highly correlated with increases in PeCO2 (r = 0.90). Esophageal tonometry may, therefore, serve as a practical alternative to gastric tonometry.

gastric partial pressure of carbon dioxide; esophageal partial pressure of carbon dioxide; gastric tonometry; rat

INTRODUCTION

MEASUREMENT OF GASTRIC WALL PCO2 has emerged as an attractive option for estimating gastrointestinal ischemia during circulatory shock states (3, 20). Because CO2 freely diffuses from gastric wall to gastric lumen, gastric wall PCO2 may be estimated from measurements of gastric luminal PCO2 by utilizing a gastric tonometer (7, 8, 15, 16). However, the PCO2 of gastric juice may in some instances exceed that of the gastric wall and of gastric venous blood (19). These excesses of PCO2 are generated from the action of acid gastric juice on bicarbonate contained either in the gastric juice itself or in the backflow of alkaline duodenal contents. The CO2 so generated also backdiffuses into the gastric mucosa, which may further increase tissue PCO2 independently of changes in mucosal blood flow (19). After H2-receptor blockade by cimetidine, H+ production by the stomach is curtailed and the PCO2 of gastric luminal fluid and that of gastric venous blood are approximately the same (11, 19). Accordingly, H2-receptor blockade is recommended as a routine to ensure reliability of conventional gastric tonometry (9, 11). Although H2-receptor blockade was previously a routine for prevention of stress ulceration in critically ill and injured patients, adverse effects, including increased risks of nosocomial pneumonia, prompted its more restrained use (4).

These limitations of gastric tonometry prompted our search for alternative sites for the measurement of visceral PCO2. Initial trials in pigs demonstrated that there were significant increases in esophageal wall PCO2 during hemorrhagic shock when these were directly measured with an ion-sensitive field-effect transistor (ISFET) PCO2 sensor. Accordingly, we were attracted to the possibility that the incorporation of an ISFET or comparable PCO2 sensor in the esophageal portion of the conventional gastric tube may serve as a competent monitor of visceral ischemia and, in turn, of the severity of perfusion failure (shock). Such esophageal measurements would potentially obviate the need for H2-receptor blockade. The present study was, therefore, undertaken to examine the relationship between gastric wall and esophageal luminal PCO2 before, during, and after reversal of hemorrhagic shock.

METHODS

The experiments were performed in an established rodent model of hemorrhagic shock (15, 20-22). All animals received humane care in compliance with the Principles of Laboratory Animal Care formulated by the National Society for Medical Research and the National Institutes of Health (NIH) Guide for the Care and Use of Laboratory Animals [DHHS Publication No. 86-32, Revised 1985, Office of Science and Health Reports, Bethesda, MD 20892].

Animal preparation. Ten Sprague-Dawley rats, weighing between 450 and 550 g, were fasted overnight except for free access to water. The animals were anesthetized by intraperitioneal injection of 45 mg/kg pentobarbital sodium supplemented with additional doses of 10 mg/kg at hourly intervals as needed. The trachea was surgically exposed at a site 2 cm caudal to the larynx. A 14-gauge cannula (Quick-Cath, Vicra Division, Travenol Laboratories, Dallas, TX) was then advanced into the trachea for a distance of 1 cm. Animals were breathing room air spontaneously. Through the left external jugular vein, a polyethylene catheter (PE-50; Becton-Dickinson, Franklin Lakes, NJ) was advanced into the right atrium for measurement of right atrial pressures. This catheter was also used as a site for injection of indicator for measurement of cardiac output. Through the left carotid artery, a polyethylene catheter was advanced into the ascending aorta for measurement of aortic pressures and for sampling aortic blood. Aortic and right atrial pressures were measured with reference to the midchest with high-sensitivity transducers (model 42584-01, Abbott Critical Care Systems, North Chicago, IL). Through the left femoral artery and left femoral vein, polyethylene catheters were advanced into the thoracic aorta and into the inferior vena cava. The left femoral arterial catheter was connected to the barrel of a standard 20-ml plastic syringe that served as a reservoir for shed blood (21, 22). The left femoral vein catheter served as a source of sampling venous blood and as a site for transfusion of blood. For measurement of cardiac output, a 1.5-Fr thermocouple microprobe (model 9030-12-D-30, Columbus Instruments, Columbus, OH) was advanced into the thoracic aorta through the right femoral artery by methods previously documented (2, 3, 17). Blood temperature was measured with this sensor and maintained between 36.5 and 37.5°C by utilizing infrared heating lamps.

For continuous measurement of esophageal luminal PCO2, a 5-Fr cannula was advanced from the mouth into the proximal esophagus. An ISFET sensor (model CO-1035, Nihon Kohden, Tokyo, Japan) was then advanced through the esophageal cannula for a distance of 12.5 cm into the lower esophagus such that the tip of the sensor was positioned ~1.5 cm proximal to the gastroesophageal junction. The cannula was then removed. A surgical incision was then made in the upper abdomen, and the stomach was exposed. An additional ISFET sensor was imbedded in the anterior wall of the gastric corpus to a depth of ~5 mm for continuous measurement of gastric wall PCO2, as previously described (3, 15, 20). This allowed for measurement of gastric wall PCO2 without interference by the gastric secretions in the lumen of the stomach. The abdomen was then closed in one layer. The validity of ISFET measurements and comparisons with conventional gastric balloon tonometry have been previously reported (2, 15).

A conventional lead II electrocardiogram was continuously recorded, utilizing subcutaneous needle electrodes. Catheters were flushed intermittently with physiological salt solution containing 2.5 IU/ml of crystalline bovine heparin.

For measurement of the regional organ blood flow by utilizing the colored-microspheres technique, an additional polyethylene catheter was advanced through the right carotid artery into the left ventricle in an additional five animals, guided by the morphology of the pressure pulses during transit from the aorta to the left ventricle. This catheter served as the injection site of colored microspheres. For withdrawal of reference blood, an additional polyethylene catheter was advanced through the right femoral artery into the thoracic aorta in lieu of the thermocouple microprobe.

Experimental procedure. The animals were randomized to serve as either hemorrhagic shock or sham controls by the sealed-envelope method. Blood from the left femoral arterial catheter was allowed to flow into the barrel of a 20-ml syringe serving as a plastic reservoir. The reservoir was pressurized to 80 mmHg for 10 min, 70 mmHg for 20 min, 60 mmHg for 20 min, and 50 mmHg for the ensuing 70 min. The reservoir pressure was controlled with a special device consisting of a piston that was manually adjusted with a lead screw, a bleeding valve, and a mercury manometer allowing for fine adjustments. After 2 h, the pressure in the reservoir was increased to 200 mmHg such that the blood in the reservoir was reinfused over an interval of 10 min. Control animals were identically treated, except that no blood was allowed to flow from the femoral arterial catheter into the reservoir. An autopsy was routinely performed in all animals, with gross inspection of thoracic and abdominal organs to identify adverse effects of the interventions.

Organ blood flow was measured with an adaptation of the colored-microspheres technique as previously described by our group and by others (5, 10, 20). Approximately 5 × 105 colored microspheres with mean diameter of 15 ± 2 µm labeled with blue, orange, green, or red (E-Z TRAC, Los Angeles, CA) were suspended in 0.1 ml of normal saline and injected into the left ventricle of the 5 additional animals over an interval of 15 s. Measurements of organ blood flow were obtained before, 60 and 120 min after the start of hemorrhage, and 60 min after reinfusion of shed blood. The reference blood was withdrawn from the thoracic aorta with a syringe pump (model 940, Harvard Apparatus, South Natick, MA) at a rate of 1 ml/min over an interval of 4 min, beginning 30 s before microsphere injection. An equal amount of donor blood was simultaneously infused into the inferior vena cava by utilizing the same syringe pump.

Both the esophagus and stomach were harvested at the end of each experiment. The wet tissue weight of each was measured with an optical balance (MAGNI-GRAD type 21, Ainsworth & Sons, Denver, CO). The organs were digested by alkaline hydrolysis in a heated water bath maintained at 50°C for 18 h. The suspension was then centrifuged at 3,000 revolutions/min for 30 min with a standard centrifuge (MARATHON 21K, Fisher Scientific, Pittsburgh, PA). The sediment containing microspheres was resuspended in the counting reagent supplied by E-Z TRAC and recentrifuged for 15 min. This sediment was then resuspended in the counting reagent such that the total volume was 0.3 ml. Aliquots of this suspension were then placed into a standard hemocytometer chamber for counting. The same procedures were applied to the reference samples of aortic blood.

Measurements. The electrocardiogram, aortic and right atrial pressures, gastric wall PCO2, and esophageal luminal PCO2 were continuously recorded with the aid of a computer (Deskpro 286, Compaq, Houston, TX) utilizing data-acquisition hardware and software (DATAQ Instruments, Akron, OH). Cardiac output was measured by the thermodilution technique after bolus injection of 200 µl of saline indicator maintained at a temperature of 15°C into the right atrium as previously described (2, 3, 17), and cardiac index was computed with the aid of a cardiac output computer (model CO-100, Institute of Critical Care Medicine, Palm Springs, CA). Aortic and right atrial blood pH, PCO2, PO2, and hemoglobin saturation were measured on a 0.7-ml sample of blood with the aid of an automated blood-gas analyzer and a CO-oximeter (models IL-1306 and IL-282, respectively, Instrumentation Laboratory, Lexington, MA). Aortic blood lactate concentrations were measured from the same sample with an electrode-based lactate analyzer (model 23L, Yellow Springs Instruments, Yellow Springs, OH). Measurements were obtained before hemorrhage (baseline measurements) and at 30, 60, 120, 150, and 180 min after the start of hemorrhage. After each blood sample had been withdrawn, an equal amount of blood from an anesthetized donor from the same litter was infused into the inferior vena cava.

Organ blood flows were computed as follows
<A><AC>Q</AC><AC>˙</AC></A>o (ml/min) = <FR><NU>C<SC>t</SC>,o &z.ccirf; <A><AC>Q</AC><AC>˙</AC></A>bw</NU><DE>C<SC>t</SC>,b</DE></FR> (1)
in which Qo is organ blood flow, CT,o is total microspheres in the organ, Qbw is flow of blood during withdrawal from the aorta (ml/min), and CT,b is total counts of blood withdrawn from the aorta
<A><AC>Q</AC><AC>˙</AC></A>ow (ml &z.ccirf; min<SUP>−1</SUP> &z.ccirf; 100 g<SUP>−1</SUP>) = <FR><NU><A><AC>Q</AC><AC>˙</AC></A>o &z.ccirf; 100</NU><DE>organ weight (g)</DE></FR> (2)
in which Qow is organ blood flow per 100 g of tissue.

Statistical analyses. Measurements are reported as means ± SD. Time-based measurements within groups were compared by analysis of variance repeated measurements. Time-coincident measurements of gastric wall PCO2 and esophageal luminal PCO2 were compared by the paired t-test. Association between gastric wall PCO2 and esophageal luminal PCO2 was examined for each animal by utilizing linear regression analysis, and the r values so obtained were averaged. A P value of <0.05 was regarded as significant.

RESULTS

Baseline measurements of mean aortic pressure, cardiac index, aortic and right atrial blood pH, PCO2 and PO2, and aortic blood lactate in both experimental and control animals (Table 1, Fig. 1) were within the physiological ranges previously reported (2, 3, 15, 20). During the 120-min interval of hemorrhage, the mean aortic pressure decreased from an average of 150 to 51 mmHg and the cardiac index from 295 to 60 ml · min-1 · kg-1 (Fig. 1). These hemodynamic changes were accompanied by increases in aortic blood lactate concentration from 0.5 to 10.7 mmol/l and in arteriovenous gradients of PCO2 from 5 to 23 Torr (Table 1). Reinfusion of shed blood restored mean aortic pressure and cardiac index to ~85% of baseline values. Concurrently, arterial lactate and arteriovenous gradients of CO2 declined.

Table 1. Acid-base and metabolic measurements before, during, and after reversal of hemorrhagic shock

Measurement Group Baseline
Hemorrhage
Reinfusion
0 min 30 min 60 min 120 min 180 min
pHa, units C 7.40 ± 0.03  7.44 ± 0.03  7.45 ± 0.03  7.44 ± 0.05  7.45 ± 0.02 
H 7.44 ± 0.02  7.48 ± 0.10  7.47 ± 0.04  7.02 ± 0.07dagger 7.29 ± 0.11*
pHv, units C 7.40 ± 0.03  7.42 ± 0.03  7.42 ± 0.04  7.44 ± 0.03  7.43 ± 0.02 
H 7.42 ± 0.03  7.46 ± 0.06  7.37 ± 0.07  6.90 ± 0.07dagger 7.19 ± 0.09dagger
PaO2, Torr C 84 ± 8  84 ± 2  86 ± 11  93 ± 7  101 ± 6 
H 91 ± 6  115 ± 19* 123 ± 16* 96 ± 25  107 ± 12 
PvO2, Torr C 53 ± 7  47 ± 9  49 ± 6  44 ± 8  45 ± 10 
H 50 ± 4  35 ± 6* 25 ± 5dagger 30 ± 12* 53 ± 9 
PaCO2, Torr C 41 ± 3  39 ± 4  36 ± 1  37 ± 4  34 ± 4 
H 37 ± 4  28 ± 10* 20 ± 5dagger 38 ± 9  22 ± 5dagger
PvCO2, Torr C 46 ± 4  43 ± 3  40 ± 5  38 ± 4  39 ± 2 
H 42 ± 4  33 ± 7dagger 29 ± 3dagger 60 ± 15* 36 ± 6 
SaO2, %  C 91 ± 2  92 ± 2  90 ± 1  93 ± 1  93 ± 2 
H 93 ± 3  95 ± 1* 96 ± 2* 82 ± 13* 92 ± 4 
SvO2, %  C 76 ± 3  69 ± 5  72 ± 4  67 ± 3  67 ± 9 
H 73 ± 6  54 ± 17  27 ± 8dagger 19 ± 9dagger 50 ± 5*
Lactate, mmol/l C 0.5 ± 0.2  0.7 ± 0.3  0.8 ± 0.2  0.9 ± 0.6  1.2 ± 0.8 
H 0.5 ± 0.1  3.8 ± 1.5dagger 7.0 ± 1.1dagger 10.7 ± 2.6dagger 4.6 ± 1.3dagger
Values are means ± SD. C, control; H, hemorrhage; pHa, arterial pH; pHv, venous pH; PaO2, arterial PO2; PvO2, venous PO2; PaCO2, arterial PCO2; PvCO2, venous PCO2; SaO2, arterial O2 saturation; SvO2, venous O2 saturation. * P < 0.05,  dagger P < 0.01 vs. control.

Fig. 1. Mean aortic pressure (MAP) and cardiac index (CI) before, during, and after hemorrhage. Values are means ± SD; n = 5 rats in each group. BL, baseline. ** P < 0.01 vs. control
[View Larger Version of this Image (27K GIF file)]

During hemorrhage, gastric wall PCO2 increased from 47 to 116 Torr and esophageal luminal PCO2 increased from 47 to 127 Torr (Fig. 2). The differences between the two measurements were not significant. Gastric blood flow decreased from 58 to 20 ml · min-1 · 100 g-1 after 60 min of bleeding and to 12 ml · min-1 · 100 g-1 at the end of the 120-min interval before reinfusion (Table 2). There were corresponding decreases in esophageal blood flow from 44 to 12 ml · min-1 · 100 g-1 at 60 min and to 7 ml · min-1 · 100 g-1 at 120 min. Within 20 min after the start of reinfusion, both gastric wall and esophageal luminal PCO2 returned to baseline levels. The measurement of esophageal luminal PCO2 was highly correlated with that of gastric wall PCO2 for individual animals and yielded an r that ranged from 0.76 to 0.98 and averaged 0.90 ± 0.09 (P < 0.0001). Gastric and esophageal blood flow returned to ~60% of preshock levels at 60 min after reinfusion of shed blood.

Fig. 2. Comparison of changes in gastric wall PCO2 (PgCO2) and esophageal luminal PCO2 (PeCO2) during hemorrhagic shock. Values are means ± SD; n = 5 rats in each group. * P < 0.05, ** P < 0.01 vs. BL.
[View Larger Version of this Image (30K GIF file)]

Table 2. Gastric and esophageal blood flow before, during, and after reversal of hemorrhagic shock

Organ Baseline
Hemorrhage
Reinfusion
 -15 min 60 min 120 min 180 min
Stomach, ml · min-1 · 100 g-1 58 ± 18 (100) 20 ± 10dagger  (34 ± 7) 12 ± 5 (21 ± 4) 36 ± 11dagger  (62 ± 10)
Esophagus, ml · min-1 · 100 g-1 44 ± 17 (100) 12 ± 7dagger  (27 ± 6) 7 ± 3dagger  (16 ± 4) 26 ± 7* (59 ± 12)
Values are means ± SD; nos. in parentheses are percentages. * P < 0.05,  dagger P < 0.01 vs. baseline.

These findings contrasted with those of the five anesthetized control animals. Neither gastric wall PCO2 nor esophageal luminal PCO2 was altered during the entire 180-min observation interval (Fig. 2).

DISCUSSION

Earlier studies demonstrated that increases in gastric wall PCO2 serve as quantitators of onset and severity of perfusion failure during circulatory shock of diverse causes, including hemorrhage, anaphylaxis, and sepsis (3, 14, 15, 20). Gastric luminal PCO2 measured with the conventional balloon tonometer underestimated relatively rapid increases in gastric wall PCO2 measured with an implanted ISFET during hemorrhagic shock (15). Accordingly, the direct measurement of gastric wall PCO2 with an implanted ISFET had greater reliability and sensitivity (15). We, therefore, utilized the implanted ISFET as a more stringent standard for comparison with esophageal luminal PCO2.

The esophageal luminal PCO2 corresponded closely to gastric wall PCO2 (r = 0.90; P < 0.0001). This contrasted with an earlier observation in which gastric wall PCO2 and tonometrically measured gastric luminal PCO2 in this model yielded a lower correlation (r = 0.71; P < 0.01) (15). After acid secretion was blocked with ranitidine, the correlation increased only to 0.80 (P < 0.01) (15). The observed increases in both esophageal and gastric wall PCO2 during hemorrhage were closely related to the decreases in aortic pressure, cardiac output, and gastric and esophageal blood flows. Hemorrhagic shock was characterized by increases in venoarterial PCO2 and arterial lactate, changes that accompanied the decreases in cardiac output and oxygen delivery characteristic of hemorrhagic shock. The esophagus, therefore, was shown to be an appropriate alternative site in lieu of the gastric luminal site for measurements of visceral PCO2 during hemorrhagic shock. The ISFET technology, which allowed for continuous measurement and display, had the additional benefit of rapidity and ease of measurement. It obviated the need for a gastric balloon from which saline is aspirated after a 60- to 90-min time interval for equilibration. It also obviated the need for simultaneous sampling of arterial blood for in vivo measurements on the aspirated saline and on the arterial blood (8).

Blood flow to the gastrointestinal viscera is sharply and disproportionately reduced during the low-flow states of hemorrhagic and obstructive shock (14, 18). Accordingly, the PCO2 values of the organs perfused by the splanchnic circulation and especially the stomach are targeted as appropriate indicators of the adequacy of blood flow for measuring aerobic metabolism in these organs. To that extent, the gastrointestinal tract has been heralded as a canary of the body because canaries are used as the traditional monitors of hypoxia due to carbon monoxide intoxication in coal mining (1). Because the esophagus is primarily supplied by the systemic rather than by the splanchnic circuit, it was not targeted as a tissue PCO2 monitor.

Because increases in esophageal PCO2 were as great as those of the gastric wall in the present study, the question arose as to whether perfusion of the esophagus was comparably reduced. The earlier assumptions notwithstanding, such was the case. Accordingly, both increases in tissue PCO2 and decreases in blood flow were approximately the same in the stomach and in the esophagus. Because the rapidity of bleeding and the severity of hemorrhagic shock were profound in the studies herein reported, we do not exclude the possibility that this close relationship in gastric and esophageal PCO2 may not apply under conditions of lesser severity in other settings such as septic shock.

We previously demonstrated that ischemia of perfusion failure, which occurs early in the viscera, represents a dual phenomenon of tissue oxygen deficits and CO2 excesses (12). This tissue hypercarbia is best explained by buffering of excesses of hydrogen ion by bicarbonate. The excess hydrogen ions are traced to anaerobically generated lactic acid and degeneration of high-energy phosphate compounds (13). This may also be related to delayed washout of metabolites during the low-flow states of circulatory shock (15, 20).

Initially, blood gases were measured on lightly anesthetized animals breathing room air spontaneously. Under these conditions, there were borderline decreases in arterial PO2 and borderline increases in arterial PCO2 compared with mechanically ventilated animals (15). However, these decreases did not alter baseline tissue PCO2, nor was there an increase in gastric wall or esophageal luminal PCO2 in control animals over the 3-h interval of measurements.

In the practical application of the esophageal luminal PCO2 measurement, we do not exclude the possibility that either CO2 generated in the gastric lumen or reflux of gastric juice into the esophagus may also alter the esophageal measurement. However, these factors were not in evidence in the course of the present studies during which gastric acid production was uninhibited.

ACKNOWLEDGEMENTS

This study was supported, in part, by a grant from the Mary Pickford Foundation of Beverly Hills, CA, and by Jack Samuelson of La Canada, CA. Sensors and financial support were provided by Nihon Kohden Corp. of Tokyo, Japan. US Patent 5579763 was awarded for Measurement of Systemic Perfusion on December 3, 1996.

FOOTNOTES

Address for reprint requests: M. H. Weil, The Institute of Critical Care Medicine, 1695 North Sunrise Way, Bldg. #3, Palm Springs, CA, 92262-5309 (E-mail: weilm{at}aol.com).

Received 25 March 1996; accepted in final form 5 September 1996.

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