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Annals of Surgical Oncology 9:632-636 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Port Site Metastasis After Diagnostic Laparoscopy for Upper Gastrointestinal Tract Malignancies: An Uncommon Entity

Margo Shoup, MD, Murray F. Brennan, MD, Martin S. Karpeh, MD, Susan M. Gillern, BA, Ross L. McMahon, MD and Kevin C. Conlon, MD, MBA

From the Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Kevin Conlon, MD, MBA, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021; Fax: 212-717-3097; E-mail: conlonk{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The role of laparoscopy for diagnosing, staging, and treating intra-abdominal malignancies is increasing. This study was designed to examine the incidence of port site metastasis and open incision site metastasis for upper gastrointestinal tract (GI) malignancies.

Methods: From a prospective database maintained by the Department of Surgery, patients undergoing laparoscopy for upper GI malignancies were identified. Clinical outcomes and recurrences were noted.

Results: Between January 1993 and January 2001, 1965 laparoscopic procedures were identified. After those patients lost to follow-up were excluded, 1650 procedures were performed in 1548 patients. Port site implantation for all laparoscopies occurred in 13 (.79%) of 1650, with a median time to recurrence of 8.2 months. After laparotomy, open incision site recurrence occurred in 9 (.86%) of 1040 (not significant). Among the patients resected, there were 5 (.60%) of 830 port site recurrences and 7 (.84%) of 830 open incision site recurrences. At the time of diagnosis of recurrence, all of the patients with port site and five of seven with open site implantation had distant or local disease, or both, as well.

Conclusions: Port site implantation after diagnostic laparoscopy for upper GI malignancy is uncommon, does not seem to be different from open incision site recurrence, and occurs in the setting of advanced disease. Therefore, the risk of port site recurrence cannot be used as an argument against laparoscopy in upper GI malignancy.

Key Words: Laparoscopy • Port site recurrence • Gastrointestinal malignancy • Staging • Incisional recurrence


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Laparoscopy has been increasingly used to stage upper gastrointestinal tract (GI) malignancies. Benefits of laparoscopic staging include identification of metastatic disease not detected before surgery, decreased morbidity and length of hospital stay, shorter recovery, and more expedient administration of chemotherapy.1–5 Although such advantages have been demonstrated in several series, reports of recurrent disease at the laparoscopic port sites have created concern in many surgical specialties.6–8

Initial reporting of port site metastasis after laparoscopy was in patients with disseminated disease at the time of surgery.6,9 Over the last decade, a number of reports have been published, with an overwhelming number in patients with gallbladder cancer.10 Larger series with laparoscopic cholecystectomy for unrecognized gallbladder cancer yielded port site recurrences in up to 28% of patients.11 This raised many questions as to the utility and appropriateness of laparoscopy for malignant disease. Further experiences documented port site recurrences in 3.9% of laparoscopic colorectal cancer cases12 but in <1% of patients with other intra-abdominal malignancies.13 As a result, the risk of developing a recurrence at the site of the trocar insertion remains unclear.

Because diagnostic laparoscopy for staging upper GI malignancy has become more popular, identifying the incidence of port site metastasis in this group is imperative. However, to date there have been few series specifically analyzing upper GI tumors. Furthermore, it is not known whether a recurrence at a port site is a clinically relevant event or whether it occurs primarily as a result of advanced disease. The purpose of this study was to document our experience with clinically apparent port site recurrence in all patients undergoing diagnostic laparoscopy for upper GI malignancies, excluding gallbladder cancer. Our goal was to determine the true incidence of port site tumor implants in this group of patients and to determine whether such recurrences are isolated events or markers of disseminated disease.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
From a prospective database maintained by the Department of Surgery, patients undergoing diagnostic laparoscopy for upper GI carcinoma were identified. Tumor sites included in the search were gastroesophageal junction, stomach, pancreas, small-bowel, and primary hepatobiliary tumors. All patients with the diagnosis of gallbladder cancer after laparoscopic cholecystectomy at outside institutions were excluded. Patients undergoing laparoscopy for lymphoma, sarcoma, or urological or gynecological malignancies were excluded (in an attempt to clarify the incidence of port site recurrence in a specific population). Laparoscopy for colorectal metastasis to the liver was excluded as well. The search yielded 1965 laparoscopic procedures performed between January 1993 and January 2001. Of these, patients alive with less than 1 month of follow-up were excluded from the study. Therefore, 1650 procedures performed in 1548 patients were included in the analysis.

Laparoscopic procedures were performed under general anesthesia with a carbon dioxide insufflation pressure of 12 to 15 mm Hg. The patient position, number and site of port sites used, and types of instruments inserted varied depending on surgeon preference, procedure planned, and findings during surgery. Clinical, operative, and pathologic details were noted in all procedures.

Some patients had an open procedure without resection, either for palliation or because of incomplete laparoscopy. The reason for unresectable disease was documented from the operative reports. All disease resected was with an open procedure, and pathologic confirmation of cancer was made either at the time of the operation or on a preoperative biopsy. All specimens were examined in the Department of Pathology at Memorial Sloan-Kettering Cancer Center. Laparoscopic ultrasound was used at the discretion of the surgeon if no evidence of metastatic disease was noted during the initial phase of the laparoscopic exploration.

Medical records were thoroughly reviewed for all laparoscopic procedures to determine clinical course. All patients included in the analysis had follow-up physical examinations at Memorial Sloan-Kettering Cancer Center by either the surgical or medical oncologist. Detection of a port site metastasis was noted after thorough review of the patient’s outpatient progress notes. These either were confirmed by biopsy (n = 9) or were recognized by the attending surgeon or medical oncologist on physical examination (n = 4) during a follow-up visit. For the purpose of this study, if a mass was noted in the area of a previous incision, it was assumed to be a metastasis. If the patient had an open procedure with an incisional recurrence at a site where a trocar was placed, it was considered a port site recurrence. If a metastatic implant was noted at the open incision site not where a trocar was placed, it was considered an open incision recurrence. Intra-abdominal or pulmonary metastatic disease and local recurrence were documented on imaging modalities during the follow-up period. Continuous variables are presented as median and range. Fisher’s exact test was applied for significance between open incision site recurrences and port site recurrences.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Of the 1548 patients undergoing 1650 laparoscopic procedures, 53% were men and 47% were women, with a median age of 66 years (range, 16–92 years). Of the 1548 patients, 2 laparoscopic procedures were performed in 102 cases. This was for staging before and after neoadjuvant treatment. The most common tumor site was the pancreatic head. Table 1 lists the sites of disease for which the laparoscopic procedures were performed.


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  		TABLE 1. Primary disease site for all laparoscopic procedures
 
A laparoscopic procedure alone was performed in 610 (33%) cases, and an open surgery followed by laparoscopy was performed in 1040 (67%) cases. With a median follow-up of 18 months (range, 1.5–74 months), 394 patients were without evidence of disease. For the remainder, 232 were alive with disease, 61 were dead of causes other than their malignancy, and 861 were dead of disease. A port site recurrence was documented after a laparoscopic procedure in 13 (.79%) of 1650 cases. A total of 4299 trocars were inserted, for a recurrence rate of 13 (.30%) of 4299 per port site. A recurrence at the open incision site was noted in 9 (.86%) of 1040 open cases. Table 2 lists the incidence of port site and open site recurrences. Of the 830 patients undergoing a curative resection, 5 (.60%) developed a port site recurrence, and 7 (.84%) developed a recurrence at the open incision. Two patients had implants at both sites. All five of the patients with port site recurrences and five of seven of those with open site recurrences had local or distant metastatic disease at the time of the diagnosis of an incisional implant. Laparoscopic ultrasound had no effect on the development of an incisional recurrence.


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  		TABLE 2. Incidence of incisional recurrences
 
The disease site associated with a port site recurrence is listed in Table 3. The median time to develop a port site implant was 8.2 months, with a range of 15 days to 17 months. Of all 13 port site recurrences, 8 (62%) occurred in patients with documented metastatic disease at the time of laparoscopy. Three patients with gastric carcinoma developed a port site recurrence. Two of the patients had carcinomatosis at the time of laparoscopy, and the third patient had carcinomatosis at the time of diagnosis of the port site implant. Of the eight patients with pancreatic carcinoma, two had carcinomatosis and two had liver metastasis at the time of laparoscopy. Two others had developed carcinomatosis and two had developed liver metastasis when the incisional implant was noted. Both patients with ampullary or hilar cholangiocarcinoma had metastatic disease at the time of laparoscopy. The umbilical port site was involved in five patients, followed by the right upper quadrant in five and the left upper quadrant in three cases. Whether the port site involved with tumor was the same one through which a biopsy was performed was not possible to ascertain from the operative reports.


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  		TABLE 3. Port site recurrence on the basis of disease location
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Concern regarding port site recurrence after laparoscopy was first raised after a report by Dobronte et al.9 in 1978, in which a patient with malignant ascites had detectable disease at the site of the trocar 2 weeks after laparoscopy. Further reports surfaced that described port site recurrences in patients undergoing laparoscopy for widespread ovarian carcinoma.6,14 The significance of a metastatic deposit at the port site was unclear, because these patients had carcinomatosis at the time of surgery. Over the next decade, case reports of port site recurrences filled the literature. However, the majority of these reports were in patients with diffuse intra-abdominal disease at the time of the detection of the incisional metastatic deposit. Therefore, the true incidence and significance of port site metastasis remained unclear.

A number of efforts were previously made to determine the extent of the problem. These included questionnaires12,15 in which the tumor status at the time of recurrence was not reported, as well as patients with gallbladder cancer detected after laparoscopic cholecystectomy.11 Therefore, the true incidence of port site recurrence and its clinical significance after diagnostic laparoscopy for upper GI malignancy, excluding incidental gallbladder cancer, have not previously been reported in a large series.

In this study, a review of 1650 diagnostic laparoscopic procedures for upper GI malignancy revealed that only .79% of the procedures led to a port site recurrence 15 days to 17 months after surgery. Of all patients who had an open procedure after laparoscopy, .86% (9 of 1040) developed an open incision recurrence. Therefore, the true incidence of port site recurrence does not seem to be different from that of an open incision recurrence. One could argue that because all the patients underwent laparoscopy, our results reflect the aerosolization of cancer cells during pneumoperitoneum in both groups. However, our reported incidence of incision recurrence is similar to that in the study of Hughes et al.,16 in which 13 (.81%) of 1600 patients developed an open incision recurrence after open laparotomy for colon cancer. Pearlstone et al.13 published similar results in a population including all nongynecological intra-abdominal malignancies. In their subset of patients with upper GI malignancies, a port site recurrence was noted in 3 (.88%) of 339 cases.

Other reports suggest that port site recurrence is more of a concern. An international survey found that 70 (17.1%) of 409 patients having laparoscopy for nonapparent gallbladder cancer developed at least 1 port site recurrence, as did 16 (3.9%) of 412 patients having laparoscopy for colorectal cancer.12 In this study, we deliberately excluded patients with lower GI carcinomas because diagnostic laparoscopy is thought to be most useful in staging patients with upper GI malignancies. We also excluded patients with gallbladder cancer, because these patients have a known increased incidence of port site metastasis, and the role for laparoscopy with this disease is questionable.9,17

Although the probability that a patient will develop a recurrence at the either the port site or the open incision site is small, the effect it will have on outcome is unclear. In our population, 830 patients had a curative resection. Of these, five (.60%) developed a port site recurrence, and seven (.84%) developed a recurrence at the open incision site. All five of the patients with a port site recurrence and five of the seven with an open incision recurrence had additional tumor detected either locally or diffusely at the time the port site implant was noted. Therefore, every port site recurrence in this series was a marker of advanced disease, rather than an isolated implant. This is similar to the findings in an earlier, smaller series, in which 2% of the patients having laparoscopy developed a port site metastasis, all in the setting of extensive peritoneal disease.18

Several proposed theories regarding the etiology of port site recurrences have emerged during the past decade. Possible mechanisms have included tissue manipulation, tumor seeding the pneumoperitoneum, and several immunological effects.19–21 In animal and human studies, peritoneal tumor seeding has been associated with carbon dioxide pneumoperitoneum during laparoscopy,21 but several reports on tumor biology have demonstrated that tumor growth is more easily established after open laparotomy than after laparoscopy.20–23 In this series, the appearance of a wound implant after either laparoscopy or open surgery reflected the underlying aggressiveness of the disease rather than the type of operation.

In summary, port site implantation after diagnostic laparoscopy for upper GI malignancies is uncommon and does not seem to be different from open incision site recurrence. In both, incision site metastasis generally occurs in the setting of advanced disease and does not affect long-term outcome. We believe that this large series supports continued use of diagnostic laparoscopy in patients with upper GI malignancies.


   Footnotes
 
In review of 1650 diagnostic laparoscopic procedures for upper gastrointestinal tract malignancy, the incidence of port site metastasis was .80%. This was not different from the incidence of open incision site recurrences and seems to occur in the setting of widespread disease.

Received for publication January 22, 2002. Accepted for publication April 25, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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  2. McColloch P, Johnson M, Jairam R, Fischer W. Laparoscopic staging of gastric cancer is safe and affects treatment strategy. Ann R Coll Surg 1998; 80: 400–2.
  3. Jimenez RE, Warshaw AL, Rattner DW, Willett CG, McGrath D, Fernandez-del Castillo C. Impact of laparoscopic staging in the treatment of pancreatic cancer. Arch Surg 2000; 135: 409–14.[Abstract/Free Full Text]
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  5. Jarnagin WR, Bodniewicz J, Dougherty E, Conlon K, Blumgart LH, Fong Y. A prospective analysis of staging laparoscopy in patients with primary and secondary hepatobiliary malignancies. J Gastroinest Surg 2000; 4: 34–43.
  6. Stockdale AD, Pocock TJ. Abdominal wall metastasis following laparoscopy: a case report. Eur J Surg Oncol 1985; 11: 373–5.[Medline]
  7. Pezet D, Fondrinier E, Rotman N, et al. Peritoneal seeding of carcinoma of the gallbladder after laparoscopic cholecystectomy. Br J Surg 1992; 79: 230.[Medline]
  8. Fusco MA, Paluzzi MW. Abdominal wall recurrence after laparoscopic-assisted colectomy for adenocarcinoma of the colon. Report of a case. Dis Colon Rectum 1993; 36: 858–61.[CrossRef][Medline]
  9. Dobronte Z, Wittmann T, Karacsony G. Rapid development of malignant metastasis in the abdominal wall after laparoscopy. Endoscopy 1978; 10: 127–30.[Medline]
  10. Schaeff B, Paolucci V, Thomopoulos J. Port site recurrences after laparoscopic surgery. A review. Dig Surg 1998; 15: 124–34.[CrossRef][Medline]
  11. Ricardo AE, Feig BW, Ellis LM, et al. Gallbladder cancer and trocar site recurrences. Am J Surg 1997; 174: 619–23.[Medline]
  12. Paolucci V, Schaeff B, Schneider M, Gutt C. Tumor seeding following laparoscopy: international survey. World J Surg 1999; 23: 989–97.[CrossRef][Medline]
  13. Pearlstone DB, Mansfield PF, Curley SA, Kumparatana M, Cook P, Feig BW. Laparoscopy in 533 patients with abdominal malignancy. Surgery 1999; 125: 67–72.[Medline]
  14. Gleeson NC, Nicosia SV, Mark JE, Hoffman MS, Cavanagh D. Abdominal wall metastases from ovarian cancer after laparoscopy. Am J Obstet Gynecol 1993; 169: 522–3.[Medline]
  15. Wexner SD, Cohen SM. Port site metastases after laparoscopic colorectal surgery for cure of malignancy. Br J Surg 1995; 82: 295–8.[Medline]
  16. Hughes ES, McDermott FT, Polglase AI, Johnson WR. Tumor recurrence in the abdominal wall scar tissue after large-bowel cancer surgery. Dis Colon Rectum 1983; 26: 571–2.[Medline]
  17. Fong Y, Brennan MF, Turnbull A, Coit DG, Blumgart LH. Gallbladder cancer discovered during laparoscopic surgery: potential for iatrogenic tumor dissemination. Arch Surg 1993; 128: 1054–6.[Abstract]
  18. van Dijkum EJN, de Wit LT, van Delden OM, et al. Staging laparoscopy and laparoscopic ultrasonography in more than 400 patients with upper gastrointestinal carcinoma. J Am Coll Surg 1999; 189: 459–65.[CrossRef][Medline]
  19. Yamaguchi K, Hirabayashi Y, Suematsu T, Shiraishi N, Adachi Y, Kitano S. Hyaluronic acid secretion during carbon dioxide pneumoperitoneum and its association with port site metastasis in a murine model. Surg Endosc 2001; 15: 59–62.[Medline]
  20. Bouvy ND, Marquet RL, Jeekel H, Bonjer HJ. Impact of gas(less) laparoscopy and laparotomy on peritoneal tumor growth and abdominal wall metastases. Ann Surg 1996; 224: 694–701.[CrossRef][Medline]
  21. Jones DB, Guo L-W, Reinhard MK, et al. Impact of pneumoperitoneum on trocar site implantation of colon cancer in a hamster model. Dis Colon Rectum 1995; 38: 1182–8.[CrossRef][Medline]
  22. Reymond MA, Wittekind CH, Jung A, Hohenberger W, Kirchner TH, Kockerling F. The incidence of port site metastases might be reduced. Surg Endosc 1997; 11: 902–6.[Medline]
  23. Allendorf JDF, Bessler M, Horvath KD, Marvin MR, Laird DA, Whelan RL. Increased tumor establishment and growth after open vs laparoscopic bowel resection in mice. Surg Endosc 1998; 12: 1035–8.[CrossRef][Medline]



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