Surgical Management

of Diaphragm Disease in Ovarian Cancer

William Cliby, MD, and Giovanni Aletti, MD
I
n a recent report from a questionnaire to the membership
of the Society of Gynecologic Oncologists (SGO),
1
bulky
diaphragm disease was one of the three most commonly re-
ported sites of disease that resulted in suboptimal cytoreduc-
tion. Nearly half of respondents that most frequently
achieved low rates of optimal cytoreduction cited lack of
evidence that performing radical procedures improved sur-
vival.
This philosophy conicts with the longstanding belief that
volume of residual disease is one of the most important in-
dependent predictors of survival. Additionally, there is ample
data demonstrating a benet for patients treated with radical
upper abdominal procedures to achieve a low residual dis-
ease.
2,3
Widespread intra-abdominal tumor (carcinomato-
sis), large amounts of ascites, nodal metastasis, and high his-
tologic grade are all considered signs of tumor aggressiveness
and associated with poor survival. However, there is also a
strong association with most of these factors and lowoptimal
debulking rates in most series.
4-7
Thus, the question of the
relative roles of tumor biology and residual disease is unclear.
Unfortunately, no independent factors have been identied
that adequately predict either tumor resectability or biologi-
cal aggressiveness in typically advanced stage disease. Impor-
tantly, there is no method yet to a priori predict in vivo
sensitivity and thus select those patients most likely to benet
from complete surgery. Considering these observations, and
recognizing the importance of intrinsic biological behavior in
ovarian cancer, surgical cytoreduction remains the corner-
stone of management of advanced stage ovarian cancer pa-
tients.
8-10
Recognizing this, it behooves us to maximize our
ability to safely resect difcult tumors.
Several procedures have been described as feasible in the
approach to upper abdominal disease.
11-14
However, there is
much evidence suggesting limited use of these procedures.
Data fromthe National Survey of Ovarian Carcinoma in 1993
revealed that only 42% to 45% of patients primarily treated
by a gynecologic oncologist received optimal debulking.
15
The corrected rate would be lower recognizing the denition
of optimal debulking used in that study exceeded the com-
monly accepted denition today of less than 1 cm. The sur-
vey of SGO membership also suggests relative lack of treat-
ment of diaphragm disease.
1
Memorial Sloan Kettering
Cancer Center has published results demonstrating that ef-
forts to improve upper abdominal surgical experience can
signicantly impact the percentage of patients optimally and
completely cytoreduced.
16
We have progressively been mod-
ifying our own approach to diaphragmdisease and attempt to
treat it as we would disease in other locations in the abdom-
inal cavity. Initially, our attempt utilized a combination of
techniques including ablative techniques. This approach has
evolved to one focused primarily on resection. Close working
relationship with hepatobiliary surgeons has been extremely
valuable in gaining familiarity and experience in mobilization
of the liver during the learning curve. We feel that this ap-
proach is safe in patients deemed able to undergo radical
surgical procedures necessary for debulking surgery. We will
describe the technique used and the impact on survival we
have observed after such procedures.
From the Department of Obstetrics and Gynecology, Mayo Clinic, Roches-
ter, MN.
Address reprint requests to William Cliby, MD, Department of Obstetrics
and Gynecology, Mayo Clinic, Rochester, MN 55902. E-mail: cliby.
william@mayo.edu.
61 1524-153X/07/$-see front matter 2007 Elsevier Inc. All rights reserved.
doi:10.1053/j.optechgensurg.2007.06.001
Operative Technique
Figure 1 Before mobilizing the liver, little room or exposure is available to safely approach the diaphragm. As seen here
the outer muscular region of the diaphragm is only slightly visible and none of the central portion can be seen despite
strong retraction of costal margin and liver. Attempting treatment of disease utilizing only retraction is subject to risk
of uncontrollable hemorrhage if vascular injury occurs and generally results in under-treatment of disease. The midline
incision used for abdominal procedures is extended to the xyphoid process, dividing the cartilage if necessary.
62 W. Cliby and G. Aletti
Figure 2 Liver mobilization begins by division of the hepatic ligamentum teres near the abdominal wall, and then the
falciform ligament. The ligamentum teres generally requires ligation for hemostasis.
Surgical management of diaphragm disease 63
Figure 3 With downward traction on the liver, the falciform ligament is divided further in the posterior direction until
the hepatic veins are just visible.
64 W. Cliby and G. Aletti
Figure 4 The right coronary and triangular ligaments are then divided exposing the bare area of the liver and completely
freeing the liver from the peritoneal attachments to the diaphragm, posterior abdominal wall, and right kidney.
Surgical management of diaphragm disease 65
Figure 5 The liver can now be rotated medially and retracted inferiorly, allowing complete exposure to the right
hemidiaphragm. The diaphragm can be seen grossly to consist of a central tendinous portion and a peripheral portion
that is more muscular (central tendinous portion labeled D). The peritoneumoverlying the kidney (K) and adrenal (Ad)
can be seen.
66 W. Cliby and G. Aletti
Surgical management of diaphragm disease 67
There are limited descriptions in the literature of technique of
diaphragm stripping or resection. We have previously de-
scribed our technique but without the benet of graphic
display.
14
The fewreports in the literature do a cursory job of
detailing steps of liver mobilization that we emphatically be-
lieve is the key to safely performing these procedures. The
right diaphragm is more commonly involved than the left
diaphragm, and presents the greatest difculty with exposure
because of the close proximity of the liver. To obtain proper
exposure requires three steps: (1) adequate incision; (2) mo-
bilization of the liver; (3) strong retraction of the costal mar-
gin, generally through the use of a xed external retraction
device (ie, third arm retractor) as shown fully in Fig 2 and
used for all gures (Figs 1-6).
Conclusions
The question of survival benet of is always raised during
discussions of extended procedures used for cytoreduction of
ovarian cancer. We have previously shown that such proce-
dures are well tolerated with acceptable morbidity.
14
In pa-
tients with signicant lung disease and limited pulmonary
reserve this operation may carry signicant respiratory com-
promise but it is unlikely they would be candidates for radical
debulking operations. Regarding survival, intuitively if one
believes the dogma and evidence regarding a survival benet
for lower residual disease, it is difcult to argue against dia-
phragm resection. Is it more justied to resect disease in the
right colic gutter compared with disease on the diaphragm?
On the other hand, is lack of familiarity with the procedure
the critical obstacle? We have analyzed our own cohort of
patients consecutively treated to determine the impact on
survival and this was recently published.
17
Briey summariz-
ing, 244 patients were analyzed with a mean age of 64 years
(range, 24-87) and 5-year overall survival (OS) was 31.5%.
For the entire cohort, residual disease (RD) was the only
independent prognostic factor in multivariate analysis (P
0.0001) when considering other factors including demo-
graphic, intraoperative ndings and procedures performed.
For the subgroup of patients with tumor involving the dia-
phragm (N 181), patients who underwent diaphragm sur-
gery (stripping of the diaphragmatic peritoneum, full or par-
tial thickness diaphragm resection, excision of nodules or
CUSA) had improved 5-year OS relative to those that did not
(53% vs. 15%; P 0.0001). Furthermore, in multivariate
analysis of patients with diaphragm disease, both RD and
performance of diaphragmsurgery were independent predic-
tors of outcome (P 0.001). Considering the subgroup of
patients with RD 1 cm, we noted a strong survival advan-
tage for those patients who underwent diaphragm surgical
procedures (5 years survival: 55% vs. 28%; P 0.0005).
16
We believe that these data are reliable and justify these pro-
cedures given the relative safety with which they can be
achieved.
Acknowledgment
We wish to thank David A. Factor, section of illustration and
design, Mayo Clinic for his wonderful artistic help in creating
the gures for this manuscript.
4
Figure 6 A typical lesion is shown here. This particular lesion is relatively isolated, though more conuent plaques are
often encountered: the management is the same. Initially, we inspect to try to determine whether the lesion can
be completely resected by simply stripping the peritoneumof the diaphragm(A) or if a diaphragmatic resection will be
required (B). Thick or invasive lesions generally require a full thickness resection of the diaphragm: those overlying the
tendinous portion require resection as well as it is nearly impossible to strip the peritoneum over this section.
Unfortunately, it is usually not reliably predictable whether stripping will sufce or if resection is needed. Stripping is
begun by incising the peritoneum over the muscular portion of the diaphragm or over the posterior abdominal wall or
some noninvolved areas of the muscular diaphragm. The peritoneum is then stripped using sharp and cautery
dissection. The peritoneum is loosely adherent to the muscular portion of the diaphragm and more intimately fused
over the tendinous portion as noted above. We feel that attempts at destruction with either electrocautery or CUSA
carry a high risk of either perforation of the diaphragm or leaving residual disease. When a lesion is encountered that
cannot be stripped further, we grasp the lesion with long Allis clamps to evert the diaphragm, and sharp resection is
performed. Orienting the incision transversely carries less theoretical risk of transaction of branches of the phrenic
nerve owing to the pattern of innervation. The resulting defect with lung visible is shown in (B). The anesthesiology
teamis informed of the defect and resultant pneumothorax. The pleura and lung are carefully inspected using palpation
of the inner surface of the diaphragm and inspection for further disease that will preclude complete resection.
Meticulous hemostasis secured to avoid a hemothorax in the postoperative period. The diaphragmatic defect is then
closed with monolament delayed absorbable sutures in a run-lock horizontal mattress fashionalternatively inter-
rupted sutures can be used. Sutures are started at either end of the defect, meeting in the middle, but not tied at this
point. A 16 French rubber catheter is temporarily placed in the pleural space before tying the nal sutures (C). The
patient is placed in steep Trendelenburg position and low continuous suction is applied to the catheter while simul-
taneously having the anesthesia team apply and hold positive end-expiratory pressure to the lungs. The catheter is
slowly withdrawn and removed while tying down the nal sutures to evacuate the pneumothorax and allow lung
re-expansion. The diaphragmis inspected for leaks and for obvious evidence of signicant residual pneumothorax; this
is generally obvious in the steep Trendelenburg position and appears as a bellowing of the diaphragm with ventilation.
We do not place a chest tube at surgery in most patients: a post- or intraoperative chest radiograph is performed on all
cases and any signicant pneumothorax managed with a chest-tube. In the absence of pneumothorax, physical sign, or
symptoms, subsequent chest radiographs are not routinely performed. Using this approach, roughly 10% of patients
will require a chest-tube postoperatively.
68 W. Cliby and G. Aletti
References
1. Eisenkop SM, Spirtos NM: What are the current surgical objectives,
strategies, and technical capabilities of gynecologic oncologists treating
advanced epithelial ovarian cancer? Gynecol Oncol 82:489-497, 2001
2. Montz FJ, Schlaerth JB, Berek JS: Resection of diaphragmatic perito-
neum and muscle: Role in cytoreductive surgery for ovarian cancer.
Gynecol Oncol 35:338-340, 1989
3. Eisenkop SM, Spirtos NM: Procedures required to accomplish com-
plete cytoreduction of ovarian cancer: Is there a correlation with bio-
logical aggressiveness and survival? Gynecol Oncol 82:435-441, 2001
4. Potter ME, Partridge EE, Hatch KD, et al: Primary surgical therapy for
ovarian cancer: How much and when. Gynecol Oncol 40:195-200,
1992
5. Farias-Eisner R, Teng R, Olivera M, et al: The inuence of tumor grade,
distribution, and extent of carcinomatosis in minimal residual stage III
epithelial ovarian cancer after optimal primary cytoreductive surgery.
Gynecol Oncol 55:108-110, 1994
6. Le T, Krepart GV, Lotocki RJ, et al: Does debulking surgery improves
survival in biologically aggressive ovarian cancer. Gynecol Oncol 67:
208-214, 1997
7. Silvestrini R, Daidone MG, Veneroni S, et al: The clinical predictivity of
biomarkers of Stage IIIIV epithelial ovarian cancer in a prospective
randomized treatment protocol. Cancer 82:159-167, 1998
8. Grifths CT: Surgical resection of tumor bulk in the primary treatment
of ovarian carcinoma. NCI Monogr 42:101, 1975
9. Randall TC, Rubin SC: Cytoreductive surgery for ovarian cancer. Surg
Clin North Am 81:871-883, 2001
10. Hoskins WJ: Epithelial ovarian cancer: Principles of primary surgery.
Gynecol Oncol 55:S91-S96, 1994
11. Deppe G, Malviya VK, Boike G, et al: Surgical approach to diaphrag-
matic metastases from ovarian cancer. Gynecol Oncol 24:258-260,
1986
12. Brand E, Pearlman N: Electrosurgical debulking for ovarian cancer: A
new technique using the argon beam coagulator. Gynecol Oncol 39:
115-118, 1990
13. Kapnick SJ, Grifths CT, Finkler NJ: Occult pleural involvement in
stage III ovarian carcinoma: Role of diaphragm resection. Gynecol On-
col 39:135-138, 1990
14. Cliby W, Dowdy S, Feitoza SS, et al: Diaphragm resection for ovarian
cancer: Technique and short-term complications. Gynecol Oncol 94:
655-660, 2004
15. Nguyen HN, Averette HE, Hoskins W, et al: National survey of ovarian
carcinoma. Part V. The impact of physicians specialty on patients
survival. Cancer 15:72:3663-36701993
16. Eisenhauer EL, Abu-Rustum NR, Sonoda Y, et al: The addition of ex-
tensive upper abdominal surgery to achieve optimal cytoreduction im-
proves survival in patients with stages IIIC-IV epithelial cancer. Gy-
necol Oncol 103:1083-1090, 2006
17. Aletti GD, Dowdy SC, Podratz KC, et al: Surgical treatment of dia-
phragm disease correlates with improved survival in optimally de-
bulked advanced stage ovarian cancer. Gynecol Oncol 100:283-287,
2006
Surgical management of diaphragm disease 69