Port Site Metastasis and Tumor Seeding inOncologic Laparoscopic Urology
Octavio A. Castillo, and Gonzalo Vitagliano
Tumor seeding and port site metastasis remain a valid concern during laparoscopic procedures for urologic malignan-cies. A systematic review of all cases reported in published studies was performed. A MEDLINE search identified 17English studies reporting a total of 29 cases of port site metastasis or tumor seeding secondary to urologic laparoscopicprocedures in the past 20 years. Many factors contribute to port site metastases and tumor seeding. Nevertheless, webelieve that only proper preoperative criteria, along with cautious intraoperative judgment, will keep port sitemetastasis to a minimum in the future. UROLOGY 71: 372–378, 2008. 2008 Elsevier Inc.
T he oncologic safety of laparoscopic procedures for in the setting of urologic malignancies. Also, current in
malignancies has been widely questioned. Con-
vitro and in vivo studies, along with clinical trials, were
cerns about port site metastasis and tumor seeding
analyzed concerning the association of tumor seeding and
have limited the use of laparoscopy in the treatment of
port site metastasis with laparoscopy. The Mesh terms
malignancies. For many years, the mistaken belief that
used were “laparoscopy,” “urology,” “port site metastases,”
laparoscopic procedures might result in a greater inci-
“tumor seeding,” and “tumor recurrence.”
dence of tumor seeding than their open counterpart hasjustified the persecution of the laparoscopist who per-
formed these procedures in the setting of
The advantages of a minimally invasive approach have
The reported incidence of tumor seeding and port site
been well established. Shorter convalescence and de-
metastasis in the published surgical data ranges from
creased analgesic requirements, along with better cosme-
0.6% to Ziprin et al.,
as reviewed by
sis results, favor minimally invasive procedures. However,
reviewed 27 studies, each with a minimum of 50 cases,
no oncologic benefit for a minimally invasive approach to
from 1993 to 2001 and found an overall incidence of only
surgical resection of cancer has been For
0.71%. They suggested that the incidence of port site
this reason, careful patient selection is critical to keep
metastases after laparoscopic surgery was similar to that
tumor seeding to a minimum. However, laparoscopy is
seen after open However, in the urologic data,
currently used to treat an ever-increasing number of
few reports of tumor seeding and port site metastasis have
malignancies at many numerous centers worldwide with
been Rassweiler et found an incidence of
oncologic results comparable to those of open proce-
0.18% in 1098 patients who had undergone laparoscopic
procedures for urologic malignancies between 1992 and
What is the real association between tumor seeding
2002. More recently, in an international survey by Micali
and laparoscopic procedures in urology? Are there pre-
et a total of 18,750 laparoscopic procedures were
reviewed, of which 10,912 were for cancer. The inci-
It was Dobronte et in 1978 who made the first
dence of port site seeding was 0.09% (10 cases) and that
report of a port site metastasis after laparoscopy. Implan-
of peritoneal spread was 0.03% (3 cases). The investiga-
tation at the place of penetration of the pneumo-needle
tors concluded that tumor seeding after laparoscopic on-
and the trocar by the mediation of ascites-containing
cologic surgery is rare and does not appear to be greater
cells of a malignant ovarian cyst adenoma was
than what has been historically reported for open surgery.
We performed a MEDLINE search for English-lan-
In a recent review by Lee et a similar incidence was
guage studies reporting tumor seeding or port site metas-
tasis associated with laparoscopic procedures performed
At our institution, 1280 laparoscopic procedures have
been performed for malignancies in the past 10 years.
Two patients presented with tumor seeding, for an inci-
From the Section of Endourology and Laparoscopic Urology, Department of Urology,
Clínica Santa Maria; and Department of Urology, Universidad de Chile School ofMedicine, Santiago de Chile, Chile
Reprint requests: Octavio A. Castillo, M.D., F.A.C.S., Section of Endourology and
Laparoscopic Urology, Department of Urology, Clínica Santa María, Avenida Santa
María 0500, Providencia, Santiago de Chile 7530234 Chile. E-mail:
Multiple theories have tried to explain the development
Submitted: March 9, 2007, accepted (with revisions): October 26, 2007
of port site metastases. However, no single hypothesis can
be blamed as the sole cause of tumor seeding. Many
More recently, Ost et performed an extensive
factors would appear to facilitate tumor seeding in the
review on the basic physiologic responses associated with
setting of laparoscopic The factors related
pneumoperitoneum. The investigators concluded that,
to tumor seeding and port site metastases can be divided
although conflicting data exist from animal and human
in three categories: tumor related, wound related, and
studies, a general trend is present toward systemic im-
mune preservation and peritoneal immune depressionduring insufflation-based laparoscopy. This altered peri-toneal immune response could be an adverse event con-
tributing to the rare development of port site metasta-
The biologic aggressiveness of the tumor as represented
by the grade and stage might play a critical role in
Most investigators have agreed that additional studies
determining the possibility of tumor Tran-
are necessary to elucidate the immune response during
sitional cell carcinoma (TCC) grade 2 and 3 have ac-
laparoscopic procedures and how this might play a role in
counted for most port site metastases reported in urologic
the incidence of tumor seeding and port site metasta-
In an international survey on tumor seeding in
urologic laparoscopy, 7 of 13 port site metastases were rep-resented by TCC. Of the 7 cases, 4 were simple nephrec-tomies with incidental TCC and 3 were nephroureterecto-
mies for suspected TCC. All but 1 case were grade 3 tumors.
Pneumoperitoneum. In an effort to determine the role
A retrieval bag was used to extract the surgical specimen
of carbon dioxide-induced tumor cell aerosolization in
in all but 1 case (incidental TCC, Stage pT1, grade 2).
tumor seeding, Ikramuddin et attempted to docu-
The remaining 6 cases were 4 laparoscopic adrenalecto-
ment this in a human model. A suction trap filled with
mies for lung metastases (Stage pT4, grade 3) and 1
saline was attached to an insufflation site on the port, the
pelvic laparoscopic lymphadenectomy for squamous pe-
carbon dioxide effluent was directed through the saline,
nile cancer (Stage pT2, grade 3) and retroperitoneal
and the specimen was concentrated for later Papanico-
laou stain. A total of 35 specimens were obtained; of
Furthermore, in a review by Tsivian and of the 9
these 15 (37%) had malignant disease. Five patients had
reported cases of port site metastases, 7 (78%) were
carcinomatosis, and staining revealed a large number of
associated with high-stage or high-grade tumors. In the
malignant cells. Malignant cells were not found in any
present review, of the 31 reported cases, 14 (45%) cor-
other patient. One patient, who displayed cellular aero-
solization, developed a port site recurrence. The investi-gators concluded that malignant cells are aerosolized butonly during laparoscopy in the presence of carcinomatosis
Wound-Related Factors (Local Immune Response)
and that it is unlikely that tumor cell aerosolization
When the first cases of tumor seeding were reported,
contributes significantly to port site metastasis.
many investigators hypothesized over the possible immu-
In a study performed by Jingli et peritoneal lavage
nologic role of this surgical approach, and the appropri-
cytology was performed for 36 patients with colorectal
ateness of this approach was again questioned in the
cancer during colorectal laparoscopic surgery and for 45
setting of malignancy. In a clinical study by Wichmann
patients with colorectal cancer during conventional sur-
et the immunologic effect of laparoscopic and open
gery. The cytology specimens were examined twice: im-
colorectal surgery were prospectively compared. A total
mediately after opening the peritoneal cavity and just
of 70 patients with colorectal diseases were prospectively
before closure of the abdomen. Malignant cells were not
enrolled, 35 patients each for laparoscopic and open
detected in the carbon dioxide filtrate gas. The incidence
surgery, respectively. Their findings indicated a less pro-
of positive cytology findings during laparoscopic surgery
nounced pro-inflammatory response to surgical trauma in
was 33.33% in the prelavage and 8.33% in the post-
patients after minimally invasive surgery. Also, the non-
lavage. The incidence of positive cytology findings during
specific immune response appeared to be less affected by
conventional surgery was 33.33% in the prelavage and
laparoscopic surgery compared with open surgery, and the
11.11% in the postlavage. The investigators concluded
specific cell-mediated immunity was equally
that during colorectal laparoscopic surgery, the carbon
In a review by Novitsky et the net immunologic
dioxide pneumoperitoneum does not affect tumor cell
advantage of laparoscopic surgery was assessed. Many
dissemination or seeding and that the laparoscopic tech-
comparative studies of cellular immunity after laparo-
niques used in colorectal cancer surgery are not associ-
scopic and conventional surgery have demonstrated an
ated with a greater risk of intraperitoneal dissemination
immunologic advantage conferred by laparoscopy. De-
of cancer cells than the conventional technique.
creased perioperative stress could be particularly impor-
Tsivian et compared abdominal wall scar implan-
tant for oncologic patients, and this advantage translated
tation of intraabdominal inoculated tumor cells after
into diminished perioperative tumor dissemination and
laparoscopic trocar insertion and pneumoperitoneum
with standard laparotomy and the patterns of tumor
Table 1. Single reports on port site metastases and tumor seeding in urologic published studies
Stolla et 1994 1 PLND Bladder TCC pT3G2 No No Lymph node
Bangma et 1995 1 PLND PCa T3N1 No No Local spillage Radioactive strontium
Altieri et 1998 1 PLND Bladder TCC T3G2 No No No Cystectomy, patient
Ahmed et 1998 1 Nephrectomy Kidney TCC T3G3-G4 No No No CHT NSOtani et 1999 1 Nephrectomy Unsuspected TCC, G3
Fentie et 2000 1 Nephrectomy RCC T3N0G4 Yes Yes No Port site metastasis
Castilho et 2001 1 Nephrectomy RCC T1N0G2 Yes Yes Ascites Immunotherapy Dead in 8 moWang et 2002 1 Cystectomy Unsuspected SCC in
Wide excision of 3 port Alive after 18 mo
Micali et 2004 13 Adrenalectomy (4) Lung metastasis T4G3;
dissemination in the peritoneal cavity in a mouse model.
They concluded that the pneumoperitoneum does not
change the intraabdominal distribution of renal cell car-
cinoma implants and that laparotomy and trocar inser-
tion with pneumoperitoneum do facilitate scar metastasis
and, therefore, pneumoperitoneum alone cannot be in-
criminated in the pathophysiology of port site metastases
Microleakage around ports, often known as the “chim-
ney effect,” might play a role in the incidence of port site
metastasis. A greater growth of tumor in the face ofgas-leaking ports was reported by Tseng et al. as reviewed
by in a rat model. However, many investigators
have postulated that a high number of aerosolized cells
Pneumoperitoneum and wound closure technique on
port site tumor implantation was evaluated by Burns
et They implanted a standard quantity of rat mam-
mary adenocarcinoma in a flank incision in Wistar-Furth
rats. After 14 days, 1-cm incisions were made in eachanimal in three quadrants. One half of the rats were
placed into a 60-minute carbon dioxide pneumoperito-
neum. Then, the flank tumor was lacerated transabdomi-
nally in both groups. The three wound sites were ran-
domized to closure of skin; skin and fascia; and skin,fascia, and peritoneum. The abdominal wounds were
harvested en bloc on postoperative day 7. No difference
was found in implantation between the pneumoperito-
neum and no pneumoperitoneum rats. Within the no-
pneumoperitoneum group, a significant increase (P ϭ
0.03) was found in tumor implantation with skin closurealone compared with closure of all three layers. The
investigators demonstrated that the closure technique
might influence the rate of port site tumor implantation
but that the use of a carbon dioxide pneumoperitoneum
does not alter the incidence of port site tumor
In a recently published animal model, Halpin et
assessed tumor implantation at abdominal wound sites
after manipulation of a solid abdominal tumor. Human
colon cancer cells were injected into the omentum of ham-sters. The hamsters were randomized to bivalve, crush, strip,or excision, with or without a pneumoperitoneum. No sig-
nificant difference was found with or without the pneumo-
peritoneum. However, a difference was found between the
groups with and without tumor manipulation. The investi-
gators concluded that tumor implantation at trocar sites
results from spillage of tumor during manipulation and not
Several investigators have compared different insuffla-
tion gases, and even gasless laparoscopy has been studiedin animal models. The findings have been contradictory,
and many investigators found no difference in the inci-
dence of port site metastasis with gasless laparoscopy or
Surgical Technique. It has been well established that
tumor boundaries must be respected to perform an onco-
logically safe procedure. It was Mathew et al. who dem-
to tissue trauma and could be responsible for wound
onstrated that tumor manipulation increased tumor me-
Also, Mutter et evaluated the effect of tumor
manipulation during laparoscopy compared with that of
conventional laparotomy on the growth and spread of an
To our knowledge, 17 studies in English have been pub-
intraperitoneal tumor in the rat in a randomized and
lished, reporting a total of 29 cases of port site metastasis
controlled trial. They concluded that manipulation was
or tumor seeding secondary to laparoscopic urologic pro-
the main factor acting on tumor dissemination in both
cedures in the past 20 years. summarizes these
groups. However, laparoscopic surgery had a beneficial
reports, along with 2 cases from our own
effect on local tumor growth compared with laparotomy
When the cases were compared, aggressive tumor bi-
ology seemed to be the main factor associated with tumor
seeding. Most cases reported were high-grade TCC.
Lee et studied animals that underwent crushing of
Other factors such as morcellation and absence of bag
a subcapsular splenic tumor during laparoscopic explora-
retrieval might also have been present.
tion. They found a greater incidence of port site involve-ment in these animals versus those who did not undergotumor It is obvious that with increasing sur-
gical skills, unnecessary tumor manipulation can be kept
In recent years, the incidence of port site metastases re-
to a minimum. It was also Lee et who reported that
ported in urologic studies has significantly decreased. Expe-
port site metastases decreased with surgeon experience in
rienced laparoscopists and standardized techniques have al-
the same animal model. Another crucial aspect of the
lowed oncologically safe laparoscopic procedures. Despite
surgical technique is morcellation and specimen removal.
this, many investigators have studied new methods to keep
Many investigators have postulated that, when correctly
tumor seeding to a minimum. The injection of intraperito-
performed, morcellation of the surgical specimen is on-
neal agents to eradicate liberated tumor cells remains con-
The use of methotrexate, povidone-iodine,
Varkarakis et recently evaluated 56 consecutive
sodium hypochlorite, chlorhexidine-cetrimide, aspirin, and
patients who underwent radical and simple transperito-
neal laparoscopic nephrectomy. Morcellation specimens
these suggestions are unproven, and peritoneal irritation
(n ϭ 33) were extracted at the umbilical or lateral port
secondary to these agents must not be underestimated. Re-
sites and intact specimens (n ϭ 23) through an infraum-
cently, some investigators have proposed the use of heparin
bilical incision. The investigators concluded that with
as an antiadhesion agent. Pross et demonstrated that
proper technique, morcellation is safe for extracting renal
low-molecular-weight heparin given subcutaneously or
tumors. However, such a specimen can be evaluated for
combined intraperitoneal lavage and subcutaneous injec-
histologic type but not for pathologic staging, limiting its
tions significantly inhibits intraabdominal tumor growth
use with TCC. Port site seeding is rare and does not
and intraperitoneal metastasis of adenocarcinoma cells in
appear to be more frequent than with open nephrectomy.
rats undergoing laparoscopy. Instillation of antiadhesion
Although morcellation is cosmetically more desirable, in
agents has been proposed in high-risk laparoscopic proce-
the latter study, no significant advantage was found in
dures with high-grade, high-stage disease or in situations inwhich the risk factors for port site implantation have been
operating time, pain, or the duration of the hospital stay.
The choice of extraction method should be left to sur-
Tsivian and have suggested several measures to
prevent urologic port site metastasis, including (a) suffi-
However, it is logical to assume that the potential risk of
cient technical preparation, (b) avoidance of laparo-
tumor seeding is greater when morcellation is performed.
scopic surgery if ascites is present, (c) trocar fixation with
Direct dissemination of tumor by contaminated instruments
avoidance of gas leakage along the trocar, (d) avoidance
or by extraction without the use of an entrapment sac have
of tumor boundary violation, (e) cautious consideration
of morcellation, (f) use of an impermeable bag if morcel-
ber of tumor cells has been observed in ports with excessive
lation is done, (g) use of a bag for intact specimen
manipulation. Ports used by the lead surgeon have been
removal, (h) drainage placement, if needed, before abdo-
proved to have more tumor contaminant than either
men deflation, (i) povidone-iodine irrigation of the lapa-
those used by the assistants or the port used for placement
roscopic instruments, trocar, and port site wounds, and
(j) suturing of 10-mm trocar wounds.
An entrapment bag should always be used for intact
Concerning hand-assisted laparoscopy, Chen et
specimen extraction, because direct contact between sur-
recommended the use of an impermeable specimen bag
gical specimen and wound can facilitate tumor seeding.
and that surgeons should not hesitate to extend the
In this regard, the incision size plays a paramount role;
wound if resistance is met while removing the specimen
an incision to small for specimen extraction can lead
from the hand port. Also, they suggested that because of
the risk of cancer cell spillage on the gloves, the operator
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