Treatment of Malignant Pleural Mesothelioma by Surgery
Robert B. Cameron, MD
Introduction. Malignant pleural mesothelioma is a
diffuse tumor of the pleural lining that,unlike many solid tumors, does not easily
lend itself to complete surgical resection. The tumor abuts all 12 ribs
and intercostal muscles, aorta, esophagus, vertebral bodies, diaphragm,
pericardium, great vessels, thymus, and the entire visceral lung surface
(figure 1). Removal of
all these structures with true pathological clear margins (R0 resection) is
not possible. Therefore, the use of surgery in this disease requires significant
compromise of normal surgical oncology principles and a strategic plan
to remediate the inherent deficiencies in an incomplete resection.
Mesothelioma Characteristics Favoring Surgery. Surgical resection of diffuse pleural disease from solid tumor epithelial
malignancies, including lung, colon, esophageal, pancreatic, and breast
cancer almost never can be achieved due to their physically invasive nature;
however, specific mesothelioma characteristics make surgery not only feasible—but
even potentially therapeutically beneficial. Due to the mesodermal origin
of the mesothelium, mesothelioma behaves less like most other common solid
tumors with endodermal origins and more like other “mesenchymal”
tumors, such as sarcomas. Importantly, both mesotheliomas and sarcomas
grow with “pushing” rather than “infiltrative” borders and have a
pseudocapsule. This physical property allows surgeons to “pull” the tumor
off all of the pleural-covered surfaces (like removing a sarcoma through
its pseudocapsule), making operations for mesothelioma even possible.
Further, the metastatic spread of the epithelioid subtype of mesothelioma
(vs biphasic and sarcomatoid) is primarily locoregional with distant metastatic
disease occurring late. Specifically, lymph node metastases occur in 50.4%-57.6% of
epithelioid (1,2), 32%-41.7% of
biphasic (1,3), and only in a few nodes in < 28%
of sarcomatoid tumors (1). Interestingly, this is similar to the characteristics of epithelioid
sarcomas. which commonly develop lymph node metastases in 22%-45% (4-7)
while the incidence of lymph node involvement in more classical
“spindle” sarcomas is low--only 3-4%.(8,9) However, it is the relatively low rate
of distant hematogenous metastases with epithelioid tumors (vs biphasic
and sarcomatoid tumors) that favors the use of locoregional therapies,
such as surgery and radiation.
Mesothelioma Characteristics Against Surgery. Like virtually all mesenchymal tumors including the sarcomas, mesothelioma
has a high incidence of
wound seeding following invasive procedures (needle tracks and surgical incisions).
The tendency for surgical site seeding does not particularly favor surgery
and has two important implications. First, surgical biopsies should be
minimized to avoid unnecessary areas of chest wall invasion and should
be limited to an subsequently easily re-resectable area, such as the low
lateral chest wall but never the visceral pleura to avoid invasion into
the lung, mediastinal pleura, or pericardium. Secondly,
“extended” surgical resections remove natural barriers to the spread of mesothelioma
(ie., pericardium and diaphragm). This can unwittingly spread the tumor
to new previously uninvolved body cavities, such as the pericardial space
and peritoneum with marked treatment consequences.
Surgical Rationale. As noted above, surgical resection of pleural mesothelioma, no matter
how radical, cannot provide a better oncologic result than an R1 resection--resection
with microscopic residual disease. Such surgical results are almost never
accepted with other solid tumors. The question is why do surgeons persist
in “debulking” pleural mesothelioma? There are no randomized
controlled trials to provide a rationale for this practice; however, there
are several observations that seemingly support the use of surgery in
this disease. First, surgery can remove all visible disease (R1 resection)
in a high percentage of patients—116/121 (95.9%) in our UCLA experience(1)—equivalent
to an otherwise rare complete response to systemic drug therapy. Secondly,
the microscopic residual disease that remains following surgery is likely
to be controlled more easily by adjuvant therapy than gross disease. Thirdly,
the majority of mesothelioma patients still succumb to local rather than
distant metastatic disease, supporting the use of more aggressive local
therapies to prolong overall survival. Fourthly, most locally advanced
solid tumors require multimodality therapy for any chance at cure. Fifth
surgery provides a unique access to the entire locoregional tumor “bed.”
Thus, surgery can provide physical access for intraoperative adjuvant
therapies, such as photodynamic therapy; betadine lavage; hyperthermic
chemotherapy; and gene, cytokine/chemokine, and stem cell therapies, which
albeit remain unproven, are currently under investigation. Finally, multimodality
therapy utilizing aggressive surgical resection at specialized centers
like ours at UCLA, almost uniformly report long-term survival (5-15 years
or more) in surgical patients. (1,10). Similar long-term survival following
any other therapy combination is exceedingly rare, if it exists at all.
Types of Surgical Procedures. A variety of surgical procedures varying from thorascopic pleurodesis
to radical extrapleural pneumonectomy (EPP) have been utilized in patients
with malignant pleural mesothelioma. The individual procedures are outlined below:
Thorascopic Pleurodesis. The simplest procedure is a thorascopic (minimally-invasive) pleurodesis
procedure. This procedure usually serves both a diagnostic and therapeutic
function. Importantly, cytopathology and small percutaneous core needle
biopsies do not provide adequate determination of histology subtype; and
therefore an optimal biopsy often can only be provided by a thorascopic
(or open pleural biopsy, if the pleural space is fused) procedure which
can assess the extent of visceral and parietal involvement and obtain
biopsy material for definitive diagnosis—preferably from the parietal
surface near the lower chest wall (lung biopsies should be avoided at
all costs). In addition, thorascopic procedures can most reliably achieve
pleural symphysis, if at least the majority of the parietal and visceral
pleurae surfaces can appose in order to prevent symptoms of recurrent
pleural effusions. Although the most reliable method of pleurodesis, talc
poudrage, alone has been associated with a reasonable median survival
of 21 months (11,12), its accepted role remains strictly for symptomatic
palliation only. It is imperative that any biopsy or port incisions are
planned to be incorporated into a standard thoracotomy incision or chest
tube site so as to prevent chest wall wound seeding outside the area of
a planned definitive thoracotomy for resection.
Pleurectomy and Decortication (P/D). The resection of mesothelioma tumor tissue by complete removal of both
the parietal and visceral pleural surfaces is termed pleurectomy and (or
with) decortication. P/D has been used for decades, first reported in
substantial series by Worn and then Martini.(13,14) Although P/D was equivalent
to the more radical EPP in Worn’s series, many surgeons still focused
on the more radical resection, undeterred by its early high mortality
rate of 31%.(15) P/D essentially became a secondary procedure performed
only when an EPP was not possible, and was referred to simply as a “debulking”
(16) or “cytoreduction” procedure.(17) These terms both imply
that portions of the tumor knowingly were left behind by the surgeon,
a likely outcome particularly if staunch EPP advocates discovered intraoperatively
that an EPP was not possible. The exact details and the extent of resections
performed under the umbrella term, “P/D,” varies tremendously
depending on surgeon and experience. The International Association for
the Study of Lung Cancer (IASLC) and the International Mesothelioma Interest
Group (IMIG) conducted a survey of surgeons’ concepts of various
P/D procedures and made recommendations for definitions of specific P/D
terminology:(17)
- Pleurectomy and Decortication (P/D). This procedure consists of a parietal
and visceral pleurectomy removing all gross tumor (R1 resection) but without
diaphragm or pericardial resection.
- Extended Pleurectomy and Decortication (Extended P/D). This procedure consists
of a parietal and visceral pleurectomy removing all gross tumor (R1 resection)
but with the addional resection of the diaphragm and/or pericardium.
- Partial Pleurectomy: This procedure consists of a partial parietal and/or
visceral pleurectomy leaving gross tumor behind (R2 resection), primarily
for diagnostic or palliative purposes.
- “Radical” is a term commonly used to indicate either the completeness
of resection or extension of the resection to include additional tissues,
such as the pericardium and diaphragm. Due to its ambiguity, this term
was left out of the IASLC/IMIG nomenclature.
A P/D is performed by placing the patient in a standard lateral decubitus
position, often with the operative table in flexion to expand the intercostal
space and facilitate exposure. Peripheral venous access is preferred with
only 2.5% of patients at UCLA requiring central venous access due to poor
peripheral access or cardiac issues. A standard posterolateral thoracotomy
incision is made, removing the 7th rib (most surgeons). All prior biopsy and/or port sites with palpable
disease undergo re-resection but routine “en bloc” resection
as performed in EPP is not usually necessary. Then, an extrapleural dissection
plane is created and extended to the thoracic apex, carefully avoiding
injury to the great vessels and apical nerves (phrenic, vagus, sympathetic
and T1 nerve root of the brachial plexus), as well as anteriorly and posteriorly,
carefully preserving the internal mammary vessels and the azygous venous
system or aorta depending on the side of the procedure. The extrapleural
dissection then is carried down to the diaphragm and pericardium where
these structures are either preserved or resected (see Extended P/D below).
In our UCLA experience, resection of these two structures rarely was necessary
(<10% of 121 patients); however, the weakened diaphragm should be reinforced
with bovine pericardial sheets (or similar biological material) covering
the majority of the central muscular and fibrous portions. Rarely, resection
of esophageal longitudinal muscle or the aortic adventitia may be required
due to tumor invasion. The parietal pleura then is mobilized to circumferentially
around the pulmonary hilum. Level 7 and all other lymph nodes (levels
2, 4, 8, 9, 10, 11 and often 12 on the right; and levels 4, 5, 6, 8, 9,
10, 11, and often 12 on the left) are removed. To this point, the operation
is essentially identical whether a P/D or EPP is performed. The lung is
then re-inflated and placed on constant positive airway pressure (CPAP)
and a scalpel (15 blade) is used to cut through both the parietal and
visceral pleurae into the superficial lung parenchyma (figure 2). The
visceral pleura is elevated gently off the lung parenchyma of each lobe
serially. A variable number of septae, which interrupt the smooth parenchyma
of the lung surface creating lobules, determine the difficulty of decortication
which may be technically challenging in some patients, yet still achievable.
Interestingly, the number of septae present in the fissure is almost always
minimal making removal of the tumor in the pulmonary fissures almost uniformly
simple and quick often taking just a few minutes. This conflicts with
the finding in EPP series that tumor in the fissures is an indication
for EPP since it cannot be removed. After complete excision of the tumor,
the chest is vigorously irrigated to remove free microscopic cells and
adjuvant therapies may be utilized. The chest is closed with multiple
drainage catheters (usually at least 4) to prevent accumulation of loculated
fluid collections. At UCLA, 93.4% of patients are extubated in the operating
room and routinely transferred to a monitored floor with only 18.2% of
patients in our 121 patient series requiring ICU care anytime during their
hospitalization.(1) Epidural-related hypotension is the most frequent
indication for ICU care. The mortality rate varies from 0-2.5% with prolonged
air leaks (23.1-33.9% after 10 days) and atrial fibrillation (11.5%-31.4%)
reported as the most frequent complications.(1,18) The mean/median length
of stay is 8.1-10.0 days.(1,18)
Extended Pleurectomy and Decortication (Extended P/D). The complete resection of both the parietal and visceral pleural surfaces
en bloc with the diaphragm and pericardium is termed an extended P/D.
It is performed essentially the same as a P/D except the diaphragm and
pericardium are removed en bloc instead of being preserved. A variety
of materials can be used for reconstruction including Gortex but also
a variety of biological materials as well.
Partial Pleurectomy. Partial resection of tumor tissue often only just enough to expand the
lung and achieve pleurodesis is termed partial pleurectomy and has been
used in many centers as
the alternative procedure in patients who cannot undergo EPP with results
that are not directly comparable to P/D, extended P/D, or EPP. Waller,
et al. reported that thorascopic simple pleurectomy provided no benefit.(19)
Extrapleural Pneumonectomy (EPP). Although Butchart originally noted that “at first sight the margin
of tumor clearance might not appear to be any greater with radical surgery
than with palliative surgery,” EPP was felt to be superior due to
the “superior” inherent clearance of tumor from the diaphragm
and lung.(15, 16) Contradictory “truths” were claimed, including
that “although it is possible to strip the
peritoneum off the muscle of the diaphragm, it is quite impossible to do the same with the
pleura.” This is despite the pleura and peritoneum having essentially the
same histological relationship—one simply being above and the other
below the diaphragmatic muscle.(15) Furthermore, Butchart felt that “diffuse
malignant pleural mesothelioma of the pleura in the
parietal pleura appears to behave quite differently from diffuse malignant pleural
mesothelioma in the
visceral pleura in terms of invasiveness.”(15) Visceral pleura was thought
to be “inseparable from the lung,” but only more recently
was complete visceral pleurectomy attempted and successfully performed.
Instead areas of diseased visceral pleura were removed leaving behind
areas of “normal” pleura. In our UCLA experience, however,
it is virtually impossible to find any pathologically normal pleura even
in areas that appear visibly normal. These concepts and attitudes persist
even today with some surgeons insisting that pleurectomy “even with
decortication”
has to “leave tumor behind.”(15)
The initial “pleurectomy” portion of an extended P/D (see above)
combined with an intra-pericardial pneumonectomy are the essential components
of an EPP. Since both an extended P/D and EPP remove the pericardium,
the pneumonectomy can be performed inside the pericardium and accomplished
simply and expeditiously, rather than a more tedious and difficult decortication.
Following removal of the lung and pleurae, again intra-operative adjuvants
may be used. Following surgery, all patients initially are observed in
the intensive care unit (ICU) with arterial and central venous catheters,
fluid is restricted to 1 L/day, and they are not allowed oral intake until
there is return of bowel function.(25) Similar to P/D, common morbidity
includes atrial fibrillation (44.2%), prolonged intubated (7.9%), and
deep venous thrombosis (6.4%), but there were slightly more vocal cord
paralysis (6.7%) and technical complications (6.1%), such as diaphragm
patch dehiscence.(25) Due to the pneumonectomy, there also were no prolonged
air leaks and a low rate of bronchopleural fistulae (0.6%).
Outcomes and Survival. Survival comparisons are complicated by heterogeneous definitions and
methods of reporting. Patient survival may be measured from the time of
surgery, from the time of first chemotherapy (particularly with neoadjuvant
chemotherapy), and even the date of study entry. Results can be compared
in two ways: within the various techniques of P/D and between P/D and
EPP. Patient outcomes for P/D, particularly as compared to EPP, are controversial
and mired in significant variation in surgical technique as well as strong
selection, center, and surgeon biases. Reported endpoints include disease-free
survival, overall survival and frequently freedom from local versus distant
recurrence. Yet, the absence of any well-designed, prospective, randomized
clinical trials leaves all claims of surgical benefit open to debate.
- Outcomes with partial pleurectomy, P/D, and extended P/D have been examined
in detail by Cao, et al.(20) Contemporary studies with adequate reported
follow-up were classified according to the IASLC-IMIG pleurectomy classification
system. Morbidity results showed that P/D and extended P/D were nearly
identical (13-48% vs 20-43%, respectively) while the morbidity of partial
pleurectomy was slightly less (14-20%).(20) P/D and partial pleurectomy
also were identical in terms of mortality, both ranging from 0 to between
7 and 8%, while extended P/D was slightly more risky (mortality = 0-11%).(20)
Although survival statistics suggested a slight trend for longer disease-free
survival in extended P/D versus P/D (range 6-7.4 mos vs 7.2-16 mos), there
were no differences observed in median overall survival (range 8.3-26
mos vs 11.5-31.7 mos).(20); however an inferior overall median survival
(7.1-14 mos) was observed in partial pleurectomy patients (disease-free
survival not able to be measured).(20)
- Outcomes with EPP have been reported by numerous authors with some excluding
perioperative deaths and others reporting outcomes predominantly in selected
favorable patient subsets potentially distorting the true outcomes for
all patient groups. Although patients with epithelioid tumors, clear lymph
nodes, complete resection, and completion of all multimodality therapy
have the best prognosis, it is extremely difficult to preoperatively select
these patients accurately. The only randomized trial reported was the
pilot Mesothelioma And Radical Surgery (MARS) Trial performed in the U.K.
This registered patients ???) for preoperative chemotherapy, re-evaluated
??? of them following induction therapy, and then randomized the remaining
patients (50) to receive surgery (24) or best supportive care (26). The
conclusions were heavily criticized due to the small patient numbers,
high crossover rates in both directions (6/26 = 23.1% in the no surgery
arm having surgery and 5/24 (20.8%) in the EPP group did not undergo surgery),
high early EPP mortality (3/24=12.5% randomized patients or 3/19=15.8%
operated patients), a low overall median EPP survival of 14.4 months (improves
to 18 mos with chemotherapy time), and a high overall median survival
in the no surgery group of 19.5 months. Despite these criticisms, the
experience likely reflects the realities of treating general mesothelioma
patients and not those attracted to specialized treatment centers. Furthermore,
there was absolutely no data suggesting that EPP was beneficial; and in
fact, showed a significant detriment in quality of life.
- A number of retrospective reports have compared outcomes with P/D (all
types) and EPP, but to date no prospective randomized trials comparing
the two procedures exist. Regardless of practical or theoretical considerations(21),
current evidence supports the claim that P/D produces similar or better
outcomes than EPP. First, mortality (and morbidity) is greater with EPP.
In a retrospective analysis of 663 patients pooled from 3 centers, Flores
et al, showed that operative mortality was 27/385 (7%) for EPP while only
13/278 (4%) for P/D.(22) A recent meta-analysis suggested an improvement
in perioperative mortality in both procedures but a difference in favor
of P/D persisted (1.7% vs 4.5%; p<0.05).(23) Secondly, several studies
suggest an overall survival benefit to P/D. For instance, Flores documented
better median survival with P/D compared to EPP (16 mos vs 12 mos; p<0.001)
even when operative deaths were excluded.(22) This persisted in the patients
with early stage tumors (AJCC stage I and II) albeit the difference did
not reach statistical significance (p=0.07). Although a scatter plot shows
overlapping overall survival statistics reported in 17 P/D studies compared
to those reported in 20 EPP series, most ranging from 8 to 21 mos (figure
3), two recent meta-analyses strongly suggested better outcomes with P/D
over EPP.(23,24)
-
Recurrence Patterns. EPP enthusiasts have long claimed improved local control
and increased distal disease recurrence from EPP, representing a “change
in the natural history” of mesothelioma. Closer analysis of the
data from the 663 patients reported by Flores, however, is instructive.
In this collective experience from three centers, local recurrence rates
(ipsilateral chest and pericardium) of 33% for EPP and 65% for P/D were
reported and distant recurrence rates (contralateral pleura/lung, peritoneum,
bone, brain, and other) of 66% for EPP and 35% for P/D claimed.(22) An
explanation for the difference was proposed in that EPP patients more
consistently received aggressive postoperative adjuvant radiation. Yet,
the inclusion of peritoneum (EPP 57 vs P/D 24), peritoneum and chest (EPP
17 vs P/D 1), abdominal viscera (EPP 12 vs P/D4) and contralateral pleura
(EPP 49 vs 14 P/D) as
“distant” recurrences defies logic in the face of the surgical techniques. The diaphragm
and pericardium are resected in all cases of EPP while not in many of
the P/D patients. With resection of the diaphragm, the peritoneum itself
becomes the new surgical margin as does the contralateral pericardial/pleural
tissue with resection of the pericardium, making recurrences in these
area more accurately classified as marginal
“local” recurrences rather than biological
“distant” recurrences. If corrected, the extended local recurrence rates become
208/219 (95%) for EPP and 129/133 (97%) for P/D. This actually suggests
poor local control in both groups.
Summary. Current evidence strongly suggests that P/D is a better operation,
both in terms of mortality and survival; however, no operation has been
evaluated in a prospective randomized controlled clinical trial, although
a planned Mesothelioma And Radical Surgery (MARS) 2 trial, a feasibility
study comparing (extended) pleurectomy decortication to no surgery is
in final planning stages in the U.K. Clearly, successful surgery for malignant
pleural mesothelioma relies heavily on the addition of effective adjuvant
therapies. With rapidly advancing knowledge of targeted and immunologically
based treatments, successful multimodality therapy may very well be possible
soon. Hope certainly exists for the future, and it appears that surgery
will remain a part of mesothelioma treatment in the foreseeable future.
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.png)
Figure 1: This MRI shows diffuse mesothelioma essentially adjacent to every
surface inside the chest including the ribs, intercostal muscles, aorta,
esophagus, vertebral bodies, diaphragm, pericardium, great vessels, thymus, and lung
.png)
Figure 2: This intraoperative photograph shows an open thoracotomy incision
with the uncovered inflated lung at the bottom left (with the visceral
surface removed and normal lung parenchyma and alveoli exposed) and the
mass of mesothelioma tumor at the upper right as it is almost completely
extirpated from the intra-thoracic surfaces.
.png)
Figure 3: This graph compares the various studies of EPP versus P/D in
terms of median survival. The range of median survivals (x axis) is slightly
greater with EPP but overall there is no difference with the vast majority
of studies for both showing a median survival of between 8 and 21 months