DOI 10.1378/chest.102.5.1337 1992;102;1337-1341Chest

 N P Singh, F S Vargas, A Cukier, M Terra-Filho, L R Teixeira and R W Light surgery.Arterial blood gases after coronary artery bypass

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Coronary artery bypass graft (CABG) surgery adversely

affects arterial blood gas (ABC) determinations. The purposes of this study were to assess serial changes in ABCsfollowing bypass surgery and identify factors that mayinfluence these changes. Room air ABCs were obtainedpreoperatively and on days 1, 2, 4, 6, and 8 postoperatively

on 125 patients undergoing bypass surgery. Fifty-five patients (saphenous vein grafting [SVG] group) had only SVG

grafting while 70 (internal mammary artery [IMA] group)received one (60 patients) or two (10 patients) IMA grafts

in addition to the SVG grafts and were subjected topleurotomy. The mean preoperative values ( ±SD) were as

follows: Pa02, 75. 1 ±7.7 mm Hg, P(A-a)02, 20.9 ±7.5 mm

Hg; PaCO2, 33.6±4.1 mm Hg; pH, 7.43±0.04; hemoglobin, 14.8±1.4 gldl; and hematocrit, 44.2±3.9 percent.There was a large decrease in the PaO postoperatively.

The nadir for the Pa02 (55.7±6.6mm Hg) occurred on thesecond postoperative day. Eight days postoperatively, there

were still significant abnormalities; the Pa02 was 65.7 ±7.3mm Hg, the P(A-a)02 was 33.2±8.8 mm Hg; the hemoglo

bin was 10.5± 1.4 g/dl; and the hematocrit was 31.7±4.0

percent. The decrease in the Pa02 was particularly noteworthy given the large decrease in the hemoglobin andhematocrit. The changes in the Pa01 were not significantlycorrelated with the age, number of grafts, pump time,length ofanesthesia, or endotracheal intubation or smoking

history. Immediately postoperatively, changes were similar

in both groups (p>O.OS);on the second postoperative day,the Pa01 had decreased 26.9 percent in the SVG group and25.5 percent in the IMA group. However, the postoperativeabnormalities resolved more slowly in the IMA group(p<O.O5). These observations suggest that the additional

trauma to the lungs and chest wall in the IMA group

(pleurotomy, the placing of pleural drains, etc) will resultin a longer recovery time in the IMA group than in SVGgroup. (Chest 1992; 102:1337-41)

CABG= coronary artery bypass graft; IMA internal mammary artery; SVG saphenous vein grafting

I mpairment in gas exchange is one of the mostsignificant postoperative complications of coronary

artery bypass graft (CABG) surgery, a common therapeutic procedure used in the treatment of coronaryartery disease. There have been several previous

For editorial comment see page 1313

reports on pulmonary function after surgery―2but innone were arterial blood gases obtained on a dailybasis postoperatively.

Internal mammary artery (IMA) grafting has beenreported to be better than saphenous vein grafting(SVG) in regards to long-term patency rates, bettersurvival rates, and lower risk oflate myocardial infarc

1,3 Therefore, IMA grafting has been advocated

whenever indicated and technically feasible. However,there is a trade-off when IMA grafts are used in thatit has been suggested that patients with IMA graftinghave greater pulmonary shunting and worse hypoxiathan patients with SVG.2 The difference in the twogroups has been attributed to pleurotomies.2

The purposes of this study were primarily to docu

*Fmm the instituto do Coraçao,Faculty of Medicine, University ofSao Paulo, Brazil, and the Department of Medicine, VeteransAdministration Medical Center, Long Beach, Calif. and theUniversity ofCalifornia, Irvine.

Manuscript received February 12; revision accepted April 8.Reprint requests: Dt@light, VA Medical Center, 5901 East Seventh,Long Beach, CA 60822

ment the serial changes in arterial blood gases afterCABG and secondarily to identify factors that mayaffect these changes.

METHODS

The patients considered suitable for CABG surgery after coronaryangiography at the Instituto do Coraçao da Universidade de SaoPaulo, Brazil, between May 1984 and May 1986 gave informedconsent approved by the institutional review board. To be includedin this protocol, the patients had to either undergo only SVG graftswith no excessive manipulation of the pleura (SVG grc@up)oralternatively to have at least one IMA graft with pleurotomy inaddition to the SVG grafts (IMA group). We selected 125 malepatients; 55 were in the SVG group and 70 were in the IMA group.These IMA patients had received one (60 patients) or two (10patients) IMA grafts. The pleural changes that occurred in thisseries of patients has been reported previously.@

Coronary bypass grafting was carried out through a midlinesternotomy. Moderate systemic hypothermia (28°to 30°C)wasapplied and cardiopulmonary bypass was carried out with adisposable bubble oxygenator. The decision to use IMA, SVG, orboth grafts was that of the operating surgeon. Postoperatively, asmalltubewasusedinallpatientsto drainthe mediastinum.Chesttubes for draining the pleural space were used when clinicallyindicated. All chest tubes were left in place for more than 24 h andin eight patients the chest tubes were left in place for more than 48h. The patients were discharged from the hospital 10.6 ±3.0 daysafter the surgery.

All subjects underwent pulmonary function testing and had aposteroanterior (PA) and a lateral chest roentgenogram preoperatively and on the sixth postoperative day.

Forced vital capacity (FVC) and forced expiratory volume in 1 s(FEy,) were obtained with a pulmonary function analyzer (HP

CHEST I 102 I 5 I NOVEMBER, 1992 1337

ArterialBloodGasesafter CoronaryArtery BypassSurgery*Naresh P Singh, M.D.; Francisco S. Varga@ M.D.; Alberto Cukier, M.D.;Mario Terra-Filho, M.D.; L4sete R. Teixeira, M.D.; andRichard W Light, M. D. , F.C. C.P

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sw@;IMAAge,

yr58.9±7.855.4±7.5tWeight,kg69. 1 ±10.070.3±10.9Pack-years26.2±29.828.2±30.8FVC,

% predict93.7±18.497.0±15.9FEy,,% predict97.6± 19.1101.1 ±17.5Times,

mmAnesthesia375.5±88.3361.2±77.7Pump121.6±44.2117.9±39.1Intubation681.5±451.3669.9±409.7

svC GrOUp

Day n Pa02 P(A-a)O2 iiIMA

GroupPaO2P(A-a)O,

svG Group

Day n PaCO2 pHIMA

Groupii

PaCO2 pH

Table 1—¿�Subjectsand Surgery Characteristics* Table 2—MeanValues(±SD)for the 1b02 (mm Hg) andP(A-a)02 (mm Hg) Preoperatively and Postoperativejy*

Preoperative 55 75.4±8.3 21.8±7.5 70 74.9±7.3 20.8±7.6Postoperative

1 50 58.1±8.7 36.9±9.9 67 59.1±8.2 35.5±9.82 51 55.1±6.2 42.4±6.9 68 55.8±6.8 40.2±8.84 52 59.7±7.4 40.0±8.5 70 58.9±6.1 40.2±8.06 51 64.4±7.0 34.2±7.6 66 62.6±6.3 36.5±9.08 37 67.4±7.7 30.8±9.8 43 64.2±6.7 34.6±8.7

*SVG = saphenous vein grafting; IMA internal mammary artery(grafting).

mm and 121 .6 ±44.2 mm) than in the IMA group(361.2 ±77.7 mm and 117.9 ±39. 1 miii). The intubation time was also greater in the SVG group (681 .5 ±451 .3 miii) than in the IMA group (669.9 ±409.7 mm),but the differences observed in these times were notsignificant(p>0.05).

Following CABG , the PaO2 decreased an average of25 percent and the alveolar-arterial oxygen differenceincreased 100 percent, both significantly (p<0.05).The changes were most pronounced on the secondpostoperative day and then showed a gradual improvement(Table2).However,eightdayspostoperatively,there were still significant abnormalities. The decreasein PaO2 observed postoperatively was not significantly(p>0.05) correlated with the anesthesia time, thepump time, or the time that the patient was maintainedwith an endotracheal tube. The alveolar-arterial oxygen gradient showed a similar behavior. Changes in itwere not correlated significantly (p>O.O5) with theaforementioned variables.

The changes in the initial days postoperatively werevirtually identical in the SVC and IMA groups. Table2 lists the mean values ( ±SD) for the PaO2 andP(A-a)O2 preoperatively and on days 1, 2, 4, 6, and 8postoperatively for both the groups. The decreaseobserved in the Pa02 on the second postoperative daywas slightly greater in the SVC group (26.9 percent)

Table 3—MeanValues(±SD)for the PaCO@(mm Hg) andpH (Units) Preoperatively and Postoperatively*

*SVG = saphenous vein grafting; IMA internal mammary artery(grafting).

tp<0.05.

47402A)and the values were compared with the equations proposedby Knudson et al.'

The roentgenograms were evaluated retrospectively for thepresence of pulmonary atelectasis or pleural changes (pleuraleffusion if at least a costophrenic angle was blunted or pleuralthickening ifthere was a discrete vertical costal pleural line withoutconcomitant blunting of the costophrenmc angle).

Blood for arterial gas analysis (pH, PaO@, PaCO,), hemoglobin,andhematocritwasobtainedin all patientspreoperativelyandondays 1, 2, 4, 6, and 8 postoperatively. On the first postoperative daythe patients were in the intensive care unit and no intercostal chesttubes had been removed. On the second day, only eight patients(two SVC and six IMA) maintained the pleural drainage. Thepatients were in bed in a semirecumbent position. The blood wascollected after the patient had been breathing room air for 20 miiiwith no respiratory support. In a small percentage of the patients,determination of the blood gas values was not possible due totechnical problems with the blood or the analyzer. Arterial bloodgas tensions were measured using a blood gas analyzer (Instrunien

tation Laboratories). The alveolar-arterial oxygen difference wascalculated from the alveolar gas equation.6 The heniatocrit wasmeasured by the microhematocrit method and the hemoglobin wasmeasured with speetrophotonietry.

Statistical Analysis

Data are expressed as the mean ±standard deviation. The effectofage, smoking habit, times ofanesthesia, cardiopulnionary bypassor endotracheal intubation, iiuinber of vessels bypassed, and IMAgraft on the changes between the postoperative and the preoperativevalues was determined by multivariate regression analysis with thevalues of the ABCs as dependent variables. To ascertain whetherthere were statistically significant differences between the SVG orIMA groups, the changes in arterial blood gases were comparedwith the unpaired t test. Probability values less than 0.05 wereconsidered significant.

RESULTS

The groups were very comparable preoperatively(Table1).Nopatientswereexcludedasa resultofsurgical complications. In both the groups preoperatively, no one was anemic, hypoxic, or underweight,they showed normal pulmonary function test results,and had similar smoking histories. The mean ageswere unexpectedly different on a statistical basis(p<0.05), but the difference was not believed to beclinically important.

The anesthesia and extracorporeal circulation timeswere slightly greater in the SVG group (375.5 ±88.3

Preoperative 55 33.2±4.4 7.43±0.05 70 34.0±3.9 7.43±0.05Postoperative

1 50 33.9±4.8 7.45±0.05 67 35.1±4.7 7.45±0.042 51 32.2±4.3 7.47±0.05 68 33.5±3.6 7.47±0.044 52 29.9±4.9 7.48±0.05 70 30.6±4.0 7.49±0.046 51 30.9±4.3 7.46±0.04 66 30.3±3.7 7.47±0.038 37 30.6±3.4 7.46±0.03 43 30.6±4.4 7.47±0.04

*SVG = saphenous vein grafting; 1MA internal mammary artery(grafting).

1338 ABG after Coronary Artery Bypass Surgery (Singh at a!)

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Normal RoentgenogramAtelectasisPleural ChangesAtelectasisand

PleuralChangesSVG

(n=19)IMA (n'll)SVG (n=5)IMA (n=6)SVG (n=23)IMA (n34)SVG

IMA(n=8)(n=19)PaO,

PreoperativePostoperativeDecrease, %

PaCO2PreoperativePostoperativeDecrease, %72.45±8.86

63.29±6.5412.6

33.76±5.3532.31 ±5.38

4.373.06±6.38

64.14±5.5712.2

33.75±4.0831.10±3.06

7.874.40±9.96

63.20±6.0215.1

33.60±4.3731.65±4.82

5.876.85±7.63

64.50±8.2316.1

33.67±3.0831.11 ±3.33

7.675.73±6.31

64.39±7.0915.0

33.44±3.0230.77±3.70

7.975.15±7.02

63.98±6.0516.4

34.26±3.6631.35±4.01

8.576.44

±5.22 75.49±5.6559.47±4.73 57.90±4.59

22.2t 23.3f

33.69±3.13 34.45±3.6531.44±3.53 31.65±2.68

6.8 8.1

DaySVGGroupIMA

GroupnHemoglobinHematocritnHemoglobinHematocritPreoperative5514.9±1.444.3±3.97014.8±1.444.0±4.1Postoperative15010.3±1.030.7±3.66710.1±1.531.0±3.625110.5±1.131.1±3.46810.0±1.230.1±3.345210.5±1.431.5±3.77010.3±1.531.1±4.365110.8±1.532.0±3.96610.6±1.531.5±4.883710.8±1.331.7±3.84310.4±1.631.4±4.2

Table 4—MeanData (±SD) Befrre and Six Days After Coronary Artery Bypass Crafting°

*SVG= saphenous vein grafting;IMA internal mammaryartery (grafting).tp<0.05 when compared with changes in the patients with a normal chest roentgenogram, in the same group.

than in the IMA group (25.5 percent), but this difference did not achieve statistical significance. However,the recovery was faster in the SVG group. Betweenthe second and eighth postoperative day, the PaO2improved significantly (p<O.05) more in the SVGgroup (12.2 ±9.0 mm Hg) than in the IMA group(8.5±7.8mm Hg@.

Serial acid-base studies showed a persistent mildrespiratoryalkalosis(Table3).The PaCO2tendedtoincreaseon the firstdayafterthe surgeryand thendecreased to values lower than the preoperative value.The pH tended to be increased throughout the postoperative period. The changes in pH and PaCO2observed after the surgery were not influenced(p>O.05) by the length ofthe procedures.

The data were anlayzed to see if there was anyrelationship between changes in the arterial blood gasvalues and changes present on the chest roentgenogram on the sixth postoperative day (Table 4). Thechanges in the blood gases were not significantlyrelated to whether atelectasis or pleural changes werepresent. However, patients who had both atelectasisand pleural changes had greater changes in their bloodvalues.

There was an impressive decrease in hemoglobinand hematocrit after CABG. On the first postoperativeday, we observed a reduction of 31 percent of the

preoperative value (p<O.05). The hemoglobin levelremained low throughout the eight days postoperatively. Table 5 shows the hemoglobin and hematocritvalues on the preoperative and on the postoperativedays for both groups. No difference was observedbetween the two groups (p>O.05) and no relationshipwas found with the variables studied (p<O.05).

DIsCussIoN

Following myocardial revascularization there weresubstantial changes in ABGs. The nadir of PaO2decrease occurred on the second postoperative day,but eight days postoperatively there were still significant abnormalities.

After cardiac surgery there was a substantial increase in the alveolar-arterial difference. In the secondpostoperative day the increase observed in P(A-a)O2was 100 percent and eight days after the surgery, theP(A-a)O2 remained 50 percent higher than it waspreoperatively. A previous study using the multipleinert gas technique demonstrated that both ventilation-perfusion mismatching and right-to-left intrapulmonary shunting are responsible for the increasedP(A-a)O2 in these patients.7 Although the diffusingcapacity is reduced secondary to the changes in lungvolumes and interstitial edema,8 its reduction probablydoes not contribute to the increased P(A-a)02.9 Alve

Table 5—MeanValues(±SD)for the Hemoglobin (gidi) and Hematocrit (%)Preoperatively and Postoperatively*

*SVG= saphenous vein grafting;IMA internal mammaryartery (grafting).

CHEST I 102 I 5 I NOVEMBER, 1992 1339

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olar hypoventilation was not responsible for the hypoxemia since the postoperative values for PaCO2were less than the preoperative values.

Arterial hypoxemia is usual following cardiac surgery and persists through the first few weeks postoperatively.8―°The PaO2 reduction reaches a nadir onthe second postoperative day and then shows gradualimprovement. The average PaO2 eight days followingsurgery was 65.7 ±7.2 mm Hg; these changes represent a 12.5 percent decrease, which is similar to the12.0 percent decrease in PaO2 reported by Braun andcoworkers8 two weeks after surgery.

The decrease in the PaO2 is particularly noteworthygiven the large decrease (31 percent) in the hemoglobin and hematocrit noted (from 44.2 percent preoperatively to 30.5 percent on the second postoperativeday). Accordingly, during the first days after surgery,the patients experience a clinically important reduclion in the oxygen content oftheir arterial blood. Thiscan compromise the supply of 02 to the tissues andlead to significant tissue ischemia.

The postoperative decrease in the PaO2 was similarin both groups. We did not find that pleurotomy(associated with IMA grafting) led to larger changesin the arterial blood gases in the days immediatelypostoperatively. It has been suggested that the pleurashould not be opened during dissection of the IMAgraft because pleurotomy is associated with a highincidence of postoperative pulmonary complica

@ Some authors have reported larger decreases

in the ‘¿�@°2with IMA grafting,―2―3while others havereported comparable decreases with both procedures.'4@'5The present study gives no support to thecontention that the decreases in the PaO2 are greaterin the IMA groups, at least in the immediate postoperative period. Indeed, the decrease that we observedin the Pa02 on the second postoperative day wasactually slightly greater in the SVG group (26.9percent) than in the IMA group (25.5 percent). Incontrast, analysis of the data on the eighth postoperative day shows that the decrease in the IMA group(14.3 percent) was greater than that in the SVG group(10.6percent).Theimprovementobservedbetweenthe second and the eighth postoperative day wassignificantly (p<O.05) greater in the SVG group. Thissuggeststhat the additionaltrauma associatedwithIMA grafting (pleurotomy, the placing of pleuraldrains, and possible additional trauma to the chestwall) result in alonger recovery time in the IMA groupthan in SVG group.

The postoperative acid-base changes demonstrate amild respiratory alkalosis in both the IMA and SVGgroups. This alteration is possibly due to a compensatory hyperventilation in response to an importantdecrease of the oxygen levels.

The influence of preoperative or intraoperative

variables on the changes in the arterial blood gasvalues postoperatively is questionable.15.16 It has beensuggested that duration of cardiopulmonary bypasshas some relationship to postoperative problems. Alveolar flooding and increased permeability pulmonaryedema occurs more frequently when the cardiopulmonary bypass time exceeds 150 @7The meanextracorporeal circulation time observed in this studywas 117.9 ±39. 1 mm and in only 14 (11 .2 percent) of125 patients did this time exceed 150 mm. We did notobserve evidence of pulmonary edema in any of ourpatients. There was no significant relationship between pump time and changesin the arterial bloodgases (p = 0.1910).

Patients with either atelectasis or pleural changeson the sixth postoperative day did not have worseblood gas values, although if both atelectasis andpleural changes were present, the blood gas valuesdid tend to be worse (Table 4).

In conclusion, the study demonstrates that followingCABC surgery, there is a marked decrease in Pa02.The nadir of Pa02 occurs usually on the secondpostoperative day and improves subsequently butremains below preoperative values on the eighth daypostoperatively. The changes in arterial blood gases inthe first days postoperatively were very similar in thegroup receiving only SVG and those who received anIMA grafting. However, the recovery time is significanfly longer in the patients submitted to pleurotomyand IMA grafting.

REFERENCES

1 Jenkins SC, Soutar SA, Forsyth A, Keates JRW, Moxham J. Lungfunction after coronary artery surgery using the internal mammary artery and the saphenous vein. Thorax 1989; 44:209-11

2 Burgess GE, Cooper JR Jr, Marino RJ, Peuler MJ, Mills NL,Ochsner JL. Pulmonary effect of pleurotomy during and aftercoronary artery bypass with internal mammary artery versussaphenous vein grafts. J Thorac Cardiovasc Surg 1978; 76:230-34

3 Loop FD, Lytle BW, Cosgrove DM, Stewart 11W,GoormasticM, Williams GW, et al. Influence of the internal-mammaryartery graft on 10-year survival and other cardiac events. NEngI J Med 1986; 314:1-6

4 Peng MJ, VargasFS, Cukier A, Terra-Filho M, Teixeira LB.Light 11WPostoperative pleural changes after coronary revascularization: comparison between saphenous vein and internalmammary artery grafting. Chest 1992; 101:327-30

5 KnudsonRJ,SlatinRC, Lebowitz MD, BurrowsB. The maximalexpiratory flow volume curve. Amer Rev Bespir Dis 1976;113:587-600

6 MellemgaardK. The alveolar-arterialoxygen difference: its sizeandcomponents in normalman. ActaPhysiol Scand 1966;67:10-20

7 Dantzker DR. Cowenhaven WM, Willoughby WJ, Kirsh M,Bower JS. Gas exchange alterations associated with weaningfrom mechanical ventilation following coronary artery bypasssurgery. Chest 1982; 82:674-77

8 Braun SR. Birnbaum ML, Chopra PS. Pre and post-operativepulmonary function abnormalities in coronary artery revascularizationsurgery.Chest 1978;73:316-20

1340 ABO after CoronaryArtery BypassSurgery (Singh etaU

 © 1992 American College of Chest Physicians by guest on July 10, 2011chestjournal.chestpubs.orgDownloaded from

9 Matthay MA. Pathophysiology ofpulmonary edema. Clin ChestMed 1985; 6:301-14

10 ArnoldM. The surgicalanatomyof sternalbloodsupply.JThorac Cardiovasc Surg 1972; 64:596-610

11 Landymore RW, Howell F. Puhnonary complications followingmyocardial revascularization with the internal mammary arterygraft. Eur J Cardiothorac Surg 1990; 4:156-62

12 Hurlbut D, Myers ML, Lefcoe M, Goldbach M. Pleuropulmonary morbidity: internal thoracic artery versus saphenous veingraft. Ann Thorac Surg 1990;50:959-64

13 Seyfer AE, Shriver CD, Miller TB, Graeber GM. Sternal bloodflow after median sternotomy and mobilization of the internalmammary arteries. Surgery 1988; 104:899-904

14 Gass GD, Olsen GN. Pre-operative pulmonary function testing

to predictpostoperativemorbidityand mortality.Chest 1986;89:127-35

15 BerrizbeitiaLD, TesslerS.JaCObOWiIZIJ,KaplanF,BudziowiczL, CunninghamJN. Effect of sternotomy and coronary bypasssurgery ofl post-operative pulmonary mechanics. Chest 1989;96:873-75

16 Warner MA, Offord KP, Warner ME, Lennon RL, ConoverMA, Jansson-SchumacherU. Role ofpre-operative cessation ofsmoking and other factors in post-operative pulmonary complications: a blinded prospective study of coronary artery bypasspatients. Mayo Cliii Proc 1989; 64:609-16

17 Kirklin JW,BlackstoneEH, Kirkhn JK. Generalprinciplesofcardiac surgery. In: Braunwald EG, ed. Cardiovascular disease.Philadelphia: WB Saunders, 1984

AdultEchocardiographyThe Center for Medical Ultrasound, Bowman Gray School of Medicine of Wake Forest

University, will present this course January18-22, 1993. Forinformation, contact the Registrar(919-716-4505 or 1-800-277-7654.

CHEST I 102 I 5 I NOVEMBER.1992 1341

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DOI 10.1378/chest.102.5.1337 1992;102; 1337-1341Chest

N P Singh, F S Vargas, A Cukier, M Terra-Filho, L R Teixeira and R W LightArterial blood gases after coronary artery bypass surgery.

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