E xtrapleural pneumonectomy has been used in the treatment

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CHEST / 103 /4 I APRIL, 1993 / Supplement 377$

Extrapleural

Pneumonectomy

in the Setting

of a

Multimodality

Approach

to Malignant

Mesothelioma*

David

I.

Sugarbaker,

M.D.,

F.C.C.P;

StevenJ.

Mentzei

M.D.,

F.C.C.P;

Malcolm

DeCamp,

M.D.;

Thomas

j

Ljnch,

Jr.,

M.D.;

and

Gary

M.

Strauss,

M.D.

The

use ofextrapleural

pneumonectomy

in a multimodality

treatment setting for malignant pleural mesothelioma is

described, presenting first

the

right-sided

approach

and

then

the

left-sided.

This

technique

used

in a multimodality

approach

with CAP

chemotherapy

(cyclophosphamide

600

mg/rn’, doxorubicin 60 mg/rn2, cisplatin 75 mg/rn2) 5 cycles

at 3-week

intervals,

and

radiotherapy

(55 Gy radiation

to

sites of previous

bulky

disease

or residual

disease)

to treat

44 patients with

malignant

pleural

mesothelioma

resulted

in improved operative mortality and decreased length of

hospital stay. (Chest 1993; 103:3775-815)

E

xtrapleural pneumonectomy has been used in the

treat-ment of tuberculous empyema’3 and other pleural

diseases including malignant pleural mesothelioma

(MPM).-b6 Its initial use in the treatment ofMPM reportedly

resulted in relatively high operative mortality6 compared

with standard ee’7

At our institution, we have gained significant experience

over the past 8 years treating diffuse MPM with a protocol

including pleuropneumonectomy, CAP (cyclophosphamide/

doxorubicin/cisplatin) chemotherapy, and radiotherapy.

Treatment results from a series of 44 patients indicate an

advantage to identifying patients preoperatively who may

derive survival benefit from such aggressive procedures

within a multimodality treatment protocol. Our surgical

technique, which includes resecting the lung, parietal and

visceral pleura, pericardium, and diaphragm, has evolved

over the 8 years, and the associated operative mortality and

length of hospital stay have continued to decrease. Our

technique, which will be discussed, varies depending on

whether it is performed on the right or the left side, and

differs from extrapleural pneumonectomy techniques

de-scribed elsewhere 918

Patient Selection

PATIENTS AND METHODS

We base selection of patients for our procedure on the traditional

parameters for defining operability in pneumonectomy patients. It

is helpful to use forced expiratory volume in 1 second (FEy,) as

well as other dynamic spirometry testing and functional oximetry

in patient selection. In the case ofborderline patient eligibility, the use of quantitative ventilation perfusion scanning may be of

signif-icant benefit for predicting postoperative pulmonary function.

*Fmm the Harvard Medical School (Dr. Lynch) and the Division

of Thoracic Surgery (Drs. Sugarbaker, Mentzer, and DeCamp),

and Department of Medicine (Dr. Strauss), Brigham and Women’s

Hospital, Boston.

Reprint requests: Dr. Sugarbaker, Brigham & Women Hospital, 75

Francis Street, Boston 02115

Because patients ultimately receive doxorubicin as adjuvant

chem-otherap); we use preoperative echocardiography to define

ventric-ular function. We have found the echocardiogram to be helpful in

identifying patients who ll be able to tolerate not only the

pneumonectomy but also the postoperative adjuvant treatments.

Midway through the postoperative chemotherapy course, the

base-line echocardiogram is used again to detect possible cardiac toxicity

Preoperative chest magnetic resonance imaging (MRI) scanning

has been useful for determining the extent of disease and particu-larlv for visualization of the sagittal planes, demonstrating evidence ofdisease in the paravertebral sulcus or disease extending through

the diaphragm. Sagittal cuts also are significantly helpful for

predicting mediastinal involvement of the cava, esophagus, or

trachea; operative resection is precluded by any one of these

findings. In cases where transdiaphragmatic involvement is

sus-peeted but not proven, limited laparotomy is used to inspect the

liver for determination of actual invasion.

Routine preoperative echocardiography and M RI are extremely

helpful in decreasing the number of patients for whom resection is

precluded at the time of surgical exploration. Patients

Between 1980 and 1991, 44 patients were selected and enrolled

in a protocol involving extrapleural pneumonectomy used as a

means of control of the primary tumor. Participants included 35

men and 9 women, with a median age of54 years (range, 46 to 62).

We perform resection only on patients with Butchart clinical stages I and II disease, and all study subjects in this trial were judged bs

clinical preoperative criteria to have Butchart’s stage I pleural

MPM6 (tumor confined within the capsule of the parietal pleiira,’ 1#{128},involving only ipsilateral lung, pericardium, and diaphragm, and

thout regional node involvement). The treatment protocol used

at the Brigham and Women’s Hospital consisted of extrapleural

pneumonectomy, including resection of pericardium and

dia-phragm, followed by CAP chemotherapy employing

cyclophospha-mide 600 mg/m2, doxorubicin 60 mg/m2, and cisplatin 75 mg/m2.

Five chemotherapy cycles were given at 3-week intervals, followed

in turn by 55 Gy radiation to previous sites of bulky disease or to

sites of residual disease in the ipsilateral chest. At present, other adjuvant chemotherapy protocols are being developed in the United

States and Europe.’2’ Every attempt was made for as complete a

cytoreductive procedure as possible, although clean surgical

mar-gins have not been shown to be beneficial in predicting survivors of MPM.’6

SUR(;ICAL TEChNIQuE

An extended right thoracotomv along the course of the 6th rib is

the incision for right-sided pleuropneumonectomy (Fig 1)! The

incision is extended from the posteru)r aspect of the thorax,

beginning midway between the posterior scapular ridge and the

spine. The cut is carried along the bed of the 6th rib to the

costochondral junction. At this juncture, a subperiosteal resection of the 6th rib is performed to create wider exposure and facilitate

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reflection

FIGURE 1. The extended right thoracotomy incision. From

Sugar-baker et al,’ with permission.

opened, and a broad-based dissection is begun superiorly toward

the apex, using blunt and sharp techniques. The dissection is

completed along the anterior lateral aspect superiorly and then

begun in a similar fashion inferiorly and laterally to the diaphragm.

We avoid dissection posteriorly to the azygous vein until wider

exposure has been gained.

Following placement of 2 chest retractors anteriorly and posteri-orly, we continue blunt and sharp dissection up to the cupola of the lung. Care is taken to palpate the course of the subclavian artery

and maintain the plane between the parietal pleura and these

vessels. It also is important to preserve the internal mammary

artery and vein, which often pass through the extrapleural plane

superomedially. If mistaken for adhesions, these vessels can be

avulsed from either the superior vena cava or the subclavian artery.

Small adhesions are divided, staying close to the pleural plane in

the extrapleural fat.

Next, the dissection is performed immediately from the apex of

Subclavian vessels Azygos vein Superior cava . Ce cc Right main bronchus

FIGURE 2. The right main stem bronchus identified. From

Sugar-baker et al, with permission.

FIGURE 3. Dissection of the pleural envelope off the diaphragm. From Sugarbaker et al, with permission.

the lung to the azygous vein. Dissection is continued extrapleurally

until the right upper lobe and main stem bronchus are clearly

identified (Fig 2).’ With sharp as well as blunt dissection, the cava

and azygous vein are then dissected from the parietal pleural

structures, again taking care to prevent avulsing the veins. The

dissection is continued anteriorly and inferiorly to the circumfer-ential diaphragmatic margin.

The next step is placement of anasogastnc tube, which facilitates

Peritoneum

/

FIGURE 4. The pentoneum wiped off the diaphragm with asponge.

From Sugarbaker et al, with permission.

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Pulmonary

artery

Diaphragm

Visceral

pleura

welope

enic nerve

I vessels

Pericardial

incision -..--- Trachea ._I::.::::___

i.riIl

Stapler” Right main bronchus 1

h

CHEST / 103 I 4 / APRIL 1993 1Supplement 379$

Parietal

pleura

FIGURE 5. Diaphragm and pleural envelope divided lateral to

inferior cava and esophagus. From Sugarbaker et al, with permis-sion.

pal pation of the esophagus to preserve it from damage. The

diaphragm is then opened posterolaterally in a radial fashion to the

anterior medial aspect of the pericardium. We are careful to keep

the pleural envelope intact, which, in some cases requires dissection of the pleural envelope off the diaphragm prior to its division (Fig 3).

When dividing the diaphragm, care must be taken to preserve

the underlying peritoneum. We use blunt dissection to wipe the

peritoneum off the diaphragm, using a sponge stick (Fig 4).’ After

the diaphragm has been divided anterolaterally to the pericardium, it is divided along the caval and esophageal hiatuses. To facilitate this dissection, one may enter the pericardium to define the course

of the inferior vena cava through the diaphragm. The diaphragm

and pleural envelope are then dissected just lateral to the inferior

cava and esophagus (Fig 5),’ thereby completing removal of the

diaphragm.

At the next stage of the procedure, the pericardium is formally

opened anteromedially to the phrenic nerve and the hilar vessels

(Fig 6). At this point, care is taken to keep the panetal pleural

FIGURE 6. The pericardium opened anteriorly, medial to the

phrenic nerve and hilar vessels. From Sugarbaker et al,u with

permission.

FIGURE 7. The intrapericardial right pulmonary artery divided by

two staple lines. From Sugarbaker et al, with permission.

envelope intact. The main pulmonary artery is divided free from

the cava and underlying superior pulmonary vein, using two staple

lines to divide the intrapericardial right pulmonary artery (Fig

7).22 After the pulmonary artery has been divided, the superior

pulmonary veins are divided in the same manner. Next, the

pericardium is divided posterior to the hilum, thereby completing

the pericardial resection. The specimen is then elevated, and

dissection continues posterior to the pericardium and lateral to the

esophagus. Subcarinal node dissection is performed, and the main

bronchus is dissected to the carina. It is stapled with a heavy gauge bronchial stapler (Fig 8),u and the specimen is removed.

A pericardial fat pad is then raised into place over the bronchial stump, and the pericardium is closed with a prosthetic patch using

a monofilament suture (Fig 9). In the right-sided procedure, the

pericardium is always reconstructed to prevent the potentially fatal

complication of cardiac herniation. Fenestrations are made in the

patch to prevent tamponade.

The next stage of the procedure is reconstruction of the

dia-phragm. We have found that the use of impermeable membranes

FIGURE 8. The main bronchus dissected to the carina and stapled.

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Anchoring

suture

in chest

wall

380$ Extrapleural Pneumonectomy in Malignant Mesothelioma (Sugarbaker et a!)

Fat

pad

Fenestrated

patch

FIGURE 9. A pericardial fat pad sewn to cover the bronchial stump;

pericardium closed with a patch, and fenestratiorts made in the

patch. From Sugarhaker et al, with permission.

prevents rapid filling of the chest cavity by peritoneal fluid. Such rapid filling can produce mediastinal shift or tamponade in the early postoperative period, before mediastinal stabilization. If peritoneal covering remains intact after the dissection, multiple sutures of 0 vicryl are used in a reefing fashion (Fig 10) to provide strength to

the overlying peritonetim. The sutures are anchored in the chest

wall (Fig 10), and flOfurther reconstruction is needed. If, however,

the peritoneum was not spared in the procedure, we place a

prosthetic impermeable patch and sew it into place with a running monofilament 0 suture (Fig 11).

Surgical specimens are assessed in the pathology suite for

resection margins in multiple areas. An remaining gross disease,

FIGURE 10. Reconstruction of the diaphragm using multiple sutures of 0 vicryl in reefing fashion; the sutures are anchored to the chest wall. From Sugarbaker et al, with permission.

FIGURE 1 1. A prosthetic impermeable patch sewn into place where

the peritoneum has been removed. From Sugarhaker et al, with

permission.

even if limited, is outlined with clips before wound closure for

subsequent radiotherap

The chest is then closed in multiple layers to assure watertight closure. A red rubber catheter is left in the chest until the skin is

closed, and air (750 InI in women, 1,000 ml in men) is removed

from the chest before the patient leaves the operating room .In the

recover room, a chest x-ray is obtained and, ifthe mediastinum is

midline, the catheter is removed. If a mediastinal shift is seen, air

can be either instilled or removed to balance the mediastinum

before removing the catheter. Alternatively, ifoozing is present, the chest tube can remain in place to waterseal overnight.

The Left-Sided Procedure

The approach for left-sided lesions is similar to that performed on the right side. Technically we find the left-sided procedure easier, due to the absence of the caval and esophageal hiatus. There are, however, subtle differences.

Care must be taken to enter the correct plane in the preaortic

region when dissecting the medial aspect of the specimen in the

Cut edge

of

pericardium

/

Pulmonary

artery

Left lung

FIGURE 12. The pulmonary artery extrapericardial and extrapleu-ral, read to be dissected. From Sugarbaker et al, with permission.

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CHE5T / 1 03 I4 / APRIL, 1 993 / Supplement 381$

posterior region. If an incorrect retroaortic plane is entered,

bleeding will result from avulsion of the intercostal vessels. In

addition, it is important that tumor involvement of the aorta be

assessed at this time.

Once the specimen has been circumferentially dissected from

the chest wall, the diaphragm is divided along the left side in a

radial fashion. Care must be taken to spare the aorta at the hiatus.

The pericardium is then entered inferiorly, and the vessels are

identified.

In the left-sided procedure, unlike that used on the right, we

prefer to dissect the extrapleural left main pulmonary artery as it

leaves the pericardium and enters the left chest. Using two vascular staple lines, we divide the pulmonary artery in its extrapericardial, extrapleural position (Fig 12). The veins are taken from within the pericardium, and the pericardial resection is completed posteriorly.

On the left side, the left main bronchus must be dissected for a

greater distance to ensure a short bronchial stump. Just as in the

right-sided procedure, the bronchial stump is covered, the

dia-phragm reconstructed, and the chest closed. The pericardium is

not routinely reconstructed on the left side because the risk of

cardiac herniation is low. At the end of the left-sided procedure,

less air needs to be removed (500 ml in women, 750 ml in men).

Hemostasis

We encourage aggressive use of electrocautery because hemosta-sis is vital to successful completion ofextrapleural pneumonectomy.

Following completion of dissection, rapid packing of areas also is

undertaken. Following removal of the specimen, hemostatic sheets

(Surgicel, Johnson & Johnson, Arlington, Tex) are placed over the

raw chest-wall surface. Packs are then placed on them, and several

minutes of tamponade is allowed to ensure a dry closure.

CLINICAL RESULTS AND DISCUSSION

The potential prognostic significance of various factors

affecting patients with

MPM

were

evaluated

in a series

of

44 consecutive patients undergoing multimodality protocol

therapy between 1980 and 1991 . Perioperative mortality

was 4.6%, and morbidity was 30%. Survival of different

patient groups was evaluated with Cox proportional hazards

models. The following potential prognostic factors were not

found to be statistically significant for survival: presence of

gross residual tumor, microscopic tumor at the resection

margin, tumor involving pericardium, and tumor involving

diaphragm.

These findings suggest that an aggressive multimodality

regimen that includes pleural pneumonectomy can be

accomplished with acceptable morbidity and mortality.

Alternative treatment strategies, possibly involving

neoad-juvant chemotherapy and/or intracavitary chemotherapy,

could be considered in selected patients. Preoperative

identification of patients with improved prognoses should

aid in selecting patients for aggressive regimens and further

define the role of multimodality therapy in MPM.

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pleura and chest wall. In: Pleural infections. Philadelphia: WB

Saunders Co, 1986; 78-171

2 Moran JF. Surgical treatment of pulmonary tuberculosis. In:

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3 Sarot IA. Extrapleural pneumonectomy and pleurectomy in

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Chir 1974; 22:386-91

6 Butchart EG, Ashcroft T, Barnsley VC, et al. Pleuropneumo-nectomy in the management of diffuse malignant mesothelioma of the pleura: experience with 29 patients. Thorax 1976; 31:15-24

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Oncol 1981; 8:321-28

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by extrapleural pneumonectomy. In: Kittle CF. ed. Current

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Current controversies in thoracic surgery. Philadelphia: WB

Saunders Co, 1986; 68-75

11 DaValle MJ, Faber LP, Kittle CF. et al. Extrapleural

pneumo-nectomy for diffuse, malignant mesothelioma. Ann Thorac Surg

1986; 42:612-18

12 Falkson C, Alberts AS, Falkson HC. Malignant pleural

meso-thelioma treatment: the current state of the art. Cancer Treat Rev 1988; 15:231-42

13 Dogan R, Cetin C, Moldibi B, et al. Traitement chirurgical du

mesotheliome pleural. Rev Pneumol Clin 1988; 44:57-63

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chirurgia nel trattamento del mesotelioma pleurico. Chir Ital

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15 Harvey JC, Fleischman EH, Kagan R, et al. Malignant pleural

mesothelioma: a survival study. J Surg Oncol 1990; 45:40-2

16 Sugarbaker DJ, Heher EC, Lee TH, et al. Extrapleural

pneu-monectomy, chemotherapy, and radiotherapy in the treatment

of diffuse malignant pleural mesothelioma. J Thorac Cardiovasc Surg 1991; 102:10-15

17 Choi NC, Mathisen DJ, Huberman MS, et al. Cancer of the

lung. In: Osteen RT, Cady B, Rosenthal PE, et al, eds. Cancer

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23 Sugarbaker DJ, Mentzer SJ. Improved technique for hilar

Figure

FIGURE 1 . The extended right thoracotomy incision. From Sugar-

FIGURE 1 .

The extended right thoracotomy incision. From Sugar- p.2
FIGURE 2. The right main stem bronchus identified. From Sugar-

FIGURE 2.

The right main stem bronchus identified. From Sugar- p.2
FIGURE 3. Dissection of the pleural envelope off the diaphragm.

FIGURE 3.

Dissection of the pleural envelope off the diaphragm. p.2
FIGURE 4. The pentoneum wiped off the diaphragm with a sponge.

FIGURE 4.

The pentoneum wiped off the diaphragm with a sponge. p.2
FIGURE 8. The main bronchus dissected to the carina and stapled.

FIGURE 8.

The main bronchus dissected to the carina and stapled. p.3
FIGURE 5. Diaphragm and pleural envelope divided lateral to

FIGURE 5.

Diaphragm and pleural envelope divided lateral to p.3
FIGURE 6. The pericardium opened anteriorly, medial to the

FIGURE 6.

The pericardium opened anteriorly, medial to the p.3
FIGURE 7. The intrapericardial right pulmonary artery divided by

FIGURE 7.

The intrapericardial right pulmonary artery divided by p.3
FIGURE 9. A pericardial fat pad sewn to cover the bronchial stump;

FIGURE 9.

A pericardial fat pad sewn to cover the bronchial stump; p.4
FIGURE 10. Reconstruction of the diaphragm using multiple sutures of 0 vicryl in reefing fashion; the sutures are anchored to the chest wall

FIGURE 10.

Reconstruction of the diaphragm using multiple sutures of 0 vicryl in reefing fashion; the sutures are anchored to the chest wall p.4
FIGURE 1 1 . A prosthetic impermeable patch sewn into place where

FIGURE 1

1 . A prosthetic impermeable patch sewn into place where p.4
FIGURE 12. The pulmonary artery extrapericardial and extrapleu-

FIGURE 12.

The pulmonary artery extrapericardial and extrapleu- p.4

References

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