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 13. Novitsky YW, Litwin DE, and Callery MP: The net immunologic might change to a new pair of surgical gloves after re- advantage of laparoscopic surgery. Surg Endosc 18: 1411–1419,
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