Extravascular Lung Water Measured Using Single ...

Original Paper Eur Surg Res 2007;39:7–13 DOI: 10.1159/000096926

Received: June 2, 2006 Accepted after revision: September 6, 2006 Published online: November 10, 2006

Extravascular Lung Water Measured Using Single Transpulmonary Thermodilution Reflects Perioperative Pulmonary Edema Induced by Esophagectomy Y. Sato a S. Motoyama a K. Maruyama a M. Okuyama a K. Hayashi a H. Nakae b K. Tajimi b J. Ogawa a Departments of a Surgery and b Emergency Medicine, Akita University School of Medicine, Akita, Japan

Key Words Pulmonary edema Esophagectomy Esophageal cancer Extravascular lung water Transpulmonary thermodilution

vascular lung water measured using PiCCO reflects the level of postoperative pulmonary edema and predicts the pulmonary complications induced by esophagectomy with extended lymph node dissection. Copyright © 2007 S. Karger AG, Basel

Abstract Pulmonary edema is the most frequent postoperative complication following esophagectomy for thoracic esophageal cancer. We enrolled 23 patients who underwent esophagectomy with extended lymph node dissection for thoracic esophageal cancer in a prospective observational clinical trial. We used the PiCCO device to measure extravascular lung water with the aim of determining whether it correlates with the respiratory index and whether it is predictive of pulmonary complications. Based on constant criteria, the tracheal tubes of 11 patients were removed on the morning of postoperative day 1 (extubation group), while 12 patients remained intubated (intubation group). These two groups significantly differed in that all patients in the extubation group recovered without any pulmonary complications, whereas 4 patients (33%) in the intubation group developed pulmonary complications. The extravascular lung water measured using PiCCO correlated significantly with the respiratory index. In the intubation group, both extravascular lung water and respiratory index were elevated 12 h after surgery and were even higher 24 h after surgery. The extra-

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Introduction

Esophagectomy with extensive lymph node dissection for thoracic esophageal cancer is one of the most invasive surgical procedures and continues to be associated with high a morbidity, despite improvements in the surgical techniques [1, 2]. It is associated, for instance, with severe hemodynamic changes involving loss of circulating blood volume and filling of the third space during the immediate postoperative period. Consequently, there is a high incidence of pulmonary complications such as lung edema, atelectasis, and pneumonia [3–5]. Despite its frequency, however, the conditions surrounding the presentation of postoperative pulmonary edema have not been fully determined. In this regard, monitoring of extravascular lung water in cases of acute lung injury or acute respiratory distress syndrome has recently proved to be very informative and useful for predicting severe lung injuries [6–9]. Bearing in mind the respiratory complica-

Satoru Motoyama, MD Department of Surgery, Akita University School of Medicine,1-1-1 Hondo Akita 010-8543 (Japan) Tel. +81 18 884 6132, Fax +81 18 836 2615 E-Mail [email protected]

Table 1. Clinicopathological characteristics of the patients in the two study groups

Extubation group (n = 11) Age, years Operation time, min Blood loss, ml Infusion balance, ml Weight gain, kg

60.687.8 532836 6548415 4,65081,400 4.181.8

Tumor location Upper Middle Lower Depth of invasion (pT) T1 T2 T3 T4 Lymph node metastasis (pN) N0 N1 Pathological stage (UICC) I IIA IIB III IV Lymph node dissection 2 fields 3 fields Treatment before surgery None Neoadjuvant chemoradiation

Intubation group (n = 12) 66.785.1 597876 8018461 5,32081,920 3.882.3

p 0.0605 0.0193* 0.3722 0.2423 0.5994

1 7 3

3 8 1

0.3629

7 1 3 0

5 0 6 1

0.3482

8 3

6 6

0.2646

6 2 1 1 1

5 1 0 3 3

0.4952

7 4

2 10

0.0211*

11 0

10 2

0.1565

* Significant difference between two groups.

tions induced by esophagectomy with extensive lymph node dissection, these findings prompted us to study perioperative changes in the extravascular lung water using the recently developed single transpulmonary thermodilution technique. Our aim was to determine whether the extravascular lung water correlates with respiratory function and predicts clinical outcome.

Patients and Methods Twenty-three consecutive patients [1 female and 22 males, age range 51–73 years, mean age 64 8 (SD) 7 years] admitted to the Akita University Hospital between 2004 and 2005 and diagnosed as having thoracic squamous cell esophageal cancer were studied. All of these patients underwent esophagectomy with extensive lymph node dissection and reconstruction involving insertion of a gastric tube via the posterior mediastinal route. They were also

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Eur Surg Res 2007;39:7–13

monitored perioperatively using the single transpulmonary thermodilution technique (PiCCO device; Pulsion Medical Systems, Munich, Germany) from the day prior to surgery through postoperative day (POD) 2. Informed consent was obtained from all patients. Our standard operative procedure is right transthoracic esophagectomy and resection of the lesser curvature with dissection of the mediastinal (involving the periesophageal region and areas around trachea and bilateral main bronchus) and the abdominal (involving the perigastric region and areas around the celiac axis) lymph nodes [1, 10, 11]. For upper thoracic esophageal cancer, or when metastases involve neck and/or upper mediastinal lymph nodes, we add bilateral neck dissection and perform a so-called three-field lymph node dissection. With this surgical strategy, 9 patients underwent esophagectomy with two-field lymph node dissection, and 14 patients underwent three-field dissection. Following surgery, extubation criteria for the intratracheal tube were PaO2 1100 Torr with a !40% inspired fraction of oxygen (FiO2), forced vital capacity 1800 ml, and no pulmonary com-

Sato/Motoyama/Maruyama/Okuyama/ Hayashi/Nakae/Tajimi/Ogawa

5.5 5.5

5.0

5.0 4.5 4.5 4.0

4.0

3.5

3.0

3.0

RI

RI

3.5

2.5

2.5

2.0

2.0

1.5

r = 0.510

1.5

r = 0.638 1.0

1.0 0.5 0 200

a

0.5 400

600

800

1,000 1,200 1,400 1,600 1,800

0 200

EVLW (ml)

400

600

800

b

1,000 1,200 1,400 1,600 1,800 EVLW (ml)

5.5 5.0 4.5 4.0 3.5 RI

3.0 2.5 2.0

r = 0.801

1.5 1.0 0.5 0 200

Fig. 1. Correlation between extravascular lung water (EVLW) and

respiratory index (RI) in all 23 patients at all measured time points after surgery (a ; r = 0.638, p ! 0.0001) and 12 h (b ; r = 0.510, p = 0.0119) and 24 h (c ; r = 0.801, p = 0.0010) after surgery.

400

600

c

800

1,000 1,200 1,400 1,600 1,800 EVLW (ml)

plications. Based on these extubation criteria, the tracheal tubes were removed from 11 patients on the morning of POD 1 (extubation group); the remaining 12 patients remained intubated (intubation group). The clinicopathological characteristics of the patients in the two groups are summarized in table 1. Two chest drains were inserted in all patients, one in the apex of the right thoracic cavity and one above the diaphragm; they were set at a negative pressure of 10 cm H2O. The drains were removed, when the discharge became serous and the drainage fell

below 200 ml/day, with no leakage of air (after POD 3 in all patients). Fluid infusion during surgery ranged from 10 to 14 ml/ kg/h, and postoperative fluid therapy was set at approximately 2.5–3.0 ml/kg/h on PODs 0–2 and at approximately 1.8–2.0 ml/ kg/h thereafter. The body weight was measured using a Hoyer lifter (Ted Hoyer, Oshkosh, Wisc., USA) and reflected the accumulation of fluid in the third space. Blood gases were analyzed using an automated blood gas analyzer system (Chiron, Emeryville, Calif., USA). The respiratory Index was calculated using

Pulmonary Edema Induced by Esophagectomy


9

*

PCCO (l/min)

9

*

*

*

*

Mann-Whitney U test. Differences between pulse contour cardiac output, global end-diastolic volume, and extravascular lung water at the measurement points were assessed using paired t tests. The relationship between extravascular lung water and respiratory index was analyzed. Statistical analyses were carried out using Statview version 5.0 for Macintosh. p ! 0.05 was considered statistically significant.

*

8 7 6 5 4

*

GEDV (ml)

2,000

Results

1,750 1,500 1,250

EVLW (ml)

550 500

*

450

ry ur te

48

h

af h 36

af

te

rs

ur rs

ur rs te af h 24

ge

ry ge

ry ge

ry ge ur rs te af

12

h

af on So

Be

fo r

te

e

rs

su

ur

rg

ge

er

y

ry

400

Fig. 2. Changes in pulse contour cardiac output (PCCO), global end-diastolic volume (GEDV), and extravascular lung water (EVLW) measured using the PiCCO device during the perioperative period in the extubation group. The PCCO was significantly increased and the EVLW significantly reduced during the immediate postoperative period (asterisks; see text).

the following equation: respiratory index = (PAO2 – PaO2)/PaO2, where PAO2 = [(760 – 47 (atmospheric pressure)] ! FiO2 – PaCO2/0.8. The respiratory index essentially reflects the ability to oxygenate the lung. The clinicopathological profile of each patient was based on the International Union Against Cancer TNM Classification of Malignant Tumors [5th ed., 1997]. On the day prior to surgery, we inserted a central venous catheter (16 Fr) via the right subclavian vein. After induction of anesthesia, we inserted a 4-Fr arterial thermodilution catheter into the right femoral artery. Calibration was done by injecting 10 ml of an iced saline solution through the central venous catheter. Pulse contour cardiac output, global end-diastolic volume, and extravascular lung water were simultaneously measured using the PiCCO transpulmonary thermodilution technique [11]. The three parameters, as well as the respiratory index, were measured at six time points: before surgery, soon after surgery, and then 12, 24, 36, and 48 h after surgery. All results are expressed as mean values 8 SD. Categorical data were compared using the chisquared test, and continuous data were compared using the

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For the 23 patients studied, the average duration of surgery was 565 8 67 min, and the blood loss was 730 8 436 ml. The primary water balance during the operation was 4,650 8 1,399 ml, and the weight gain was 3.8 8 2.1 kg. The operation time was significantly longer in the intubation group than in the extubation group. The type of lymph node dissection (2 fields vs. 3 fields) also differed between the two groups. The amount of weight gained during the operation did not differ between the two groups (extubation group 3.7 8 2.1 kg vs. intubation group 3.8 8 2.3 kg). In all patients, the extravascular lung water correlated significantly with the respiratory index (r = 0.638, p ! 0.0001) at all measurement points after surgery (fig. 1a). The correlations 12 and 24 h after surgery are shown in figures 1b and c. In the extubation group, the pulse contour cardiac output was significantly increased during the immediate postoperative period (p ! 0.0001), but it stabilized within 12 h after surgery and then remained unchanged through POD 2 (fig. 2). The global end-diastolic volume was not elevated immediately after surgery (p = 0.1894), but it began to increase within 12 h after surgery and continued to increase through POD 2. Interestingly, the extravascular lung water was clearly reduced immediately after surgery (p = 0.0068), but it recovered to preoperative levels within 12 h after surgery and remained at that level through POD 2. The changes in extravascular lung water and respiratory index during the perioperative period in the extubation and intubation groups are shown separately in figure 3. In the extubation group, measurement of the respiratory index was unavoidably ended upon extubation, because precise FiO2 measurements were impossible. In the intubation group, both extravascular lung water and respiratory index were elevated 12 h after surgery and were even higher 24 h after surgery. All of the patients in the extubation group recovered with no pulmonary complications, whereas 4 patients (33%) in the intubation group developed pulmonary complications: 3 patients develSato/Motoyama/Maruyama/Okuyama/ Hayashi/Nakae/Tajimi/Ogawa

Extubation group

Intubation group 1,000

5.0 EVLW RI

800

5.0

4.5

EVLW RI

800

4.0

2.5

*

400

2.0

600

3.0 2.5

400

2.0

1.5

1.0 0.5

ry

ry

ry

ge

ge

ur

48

h

af

af

te

te

rs

rs

ur

ur rs te

af h 24

*

ge

ge ur rs

te af h

12

*

0

ry

ry

y ur

rg

rs

su So

on

af

fo r Be

te

e

rs te af

h

b

ge

er

ry

ry

ge ur

ge

ry ur

ge

48

h

af

te

rs

ur rs 36

h 24

12

h

af

te af

te

rs

ur

ur

ge

ge

ry

ry

y er rg

rs

su

te

e So

on

af

fo r Be

*

0

0

*

h

*

0.5

0

a

1.5 200

1.0

36

200

4.0 3.5

3.0

EVLW (ml)

600

RI

EVLW (ml)

3.5

4.5

RI

1,000

Fig. 3. Changes in extravascular lung water (EVLW) and respiratory index (RI) in the extubation group (a) and in the intubation group (b). EVLW and RI were elevated 12 h after surgery and were even higher 24 h after sur-

gery. * Significant difference among pre- and postoperative values.

Table 2. Pulmonary complications after an increase in extravas-

cular lung water

No complications Complications

Extubation group (n = 11)

Intubation group (n = 12)

11 0

8 4

p

0.0351*

* Significant difference between the two groups.

oped pneumonia that needed to be treated, and 1 patient developed severe atelectasis that required the use of a ventilator (table 2). In all 4 patients that developed pulmonary complications, an increase in extravascular lung water preceded their onset.

Discussion

We have shown that extravascular lung water measured using PiCCO reflects the level of postoperative pulmonary edema induced by esophagectomy with extended lymph node dissection. It has been previously shown [12, Pulmonary Edema Induced by Esophagectomy

13] that the monitored extravascular lung water using the transpulmonary double indicator (thermo-dye) dilution technique correlated well with survival and was an independent predictor of the prognosis in critically ill patients. Over time, however, the double indicator technique has been replaced by the transpulmonary single thermal indicator technique, because the latter is relatively noninvasive and easy to perform and has proved to be an accurate means of quantifying extravascular lung water as an index of lung water [14, 15]. Moreover, its accuracy is comparable to that of the pulmonary artery thermodilution technique for measuring cardiac output and assessing volume preload parameters in patients with sepsis, acute lung injury, burn shock, coronary artery bypass graft, and liver transplantation, among others [16– 22]. When the body is under severe stress, such as occurs with esophagectomy with extensive lymph node dissection, a hemodynamic shift can occur, during which fluid accumulates in the third space. This accumulation, which is detectable as a body weight gain and as a gradual increase in global end-diastolic volume, can induce pulmonary edema, i.e., an abnormal accumulation of fluid in the extravascular compartments of the lung [23]. We found that the extravascular lung water measured using the transpulmonary thermodilution technique correlates Eur Surg Res 2007;39:7–13

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significantly with the respiratory index as an indicator of the respiratory function. Patients who showed no significant postoperative changes in extravascular lung water or respiratory index recovered without lung edema or other pulmonary complications. By contrast, those who showed an increase in extravascular lung water on POD 1 also showed a substantial increase in their respiratory index, and some developed pulmonary complications. Measurement of the extravascular lung water using the PiCCO device thus proved to be a useful method for monitoring fluid accumulation in the lung and was predictive of the pulmonary complications that subsequently occurred. Jiao et al. [24] reported that chronic obstructive pulmonary disease is the critical factor affecting the incidence of postoperative pulmonary complications in esophageal cancer patients undergoing esophagectomy. If so, the percent-predicted forced expiratory volume in 1 s would be a good predictor of postoperative pulmonary complications. However, none of the 4 patients in our group who developed pulmonary complications were diagnosed with chronic obstructive pulmonary disease.

Although the extravascular lung water declined during the immediate postoperative period, there was no change in body weight gain or global end-diastolic volume. This initial decline is thought to be due to pulmonary transpiration during surgery, when the thorax is open and there is continuous positive airway pressure ventilation. Notably, this observation is at variance with our earlier finding that there is a significant increase in X-ray density on chest radiographs during the immediate postoperative period which correlates with the respiratory index [4]. It may be that this increase in X-ray density mainly reflects thoracic wall edema and not lung edema, but further study will be required to resolve this discrepancy. We conclude that the extravascular lung water measured using the single transpulmonary thermodilution technique correlates directly with the respiratory index and is predictive of pulmonary complications, enabling early management of patients who develop pulmonary edema following esophagectomy with extensive lymph node dissection.

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