Abstract. Background: Port site metastasis following laparoscopy for cancer is reported with increasing frequency and represents one of the most important ...
Surg Endosc (1998) 12: 1294–1296
© Springer-Verlag New York Inc. 1998
Trocar site tumor recurrences May pneumoperitoneum be responsible? E. Cavina,1 O. Goletti,1 N. Molea,2 P. Buccianti,1 M. Chiarugi,1 G. Boni,2 E. Lazzeri,2 R. Bianchi2 1 2
Department of Surgery, University of Pisa, Via Roma 67, 56100 Pisa, Italy Nuclear Medicine, University of Pisa, Via Roma 67, 56100 Pisa, Italy
Received: 11 July 1997/Accepted: 11 September 1997
Abstract Background: Port site metastasis following laparoscopy for cancer is reported with increasing frequency and represents one of the most important limitations of the technique. Methods: A scintigraphic model was utilized to evaluate a possible role of pneumoperitoneum in tumor cell dissemination. Labeled red blood cells (RBC) were injected at the level of the gallbladder bed during laparoscopic cholecystectomy (LC) performed for symptomatic cholecystolithiasis. LC was performed in two groups with standard CO2 pneumoperitoneum: in one group an endobag for retrieval of the specimen was utilized. In one group a gasless LC with endobag was performed. Results: Radioactivity in the area of the trocar introduction was observed in almost all the patients who underwent standard (CO2) LC but represented a rare event in patients treated with the gasless method. The utilization of a protective bag for the extraction of the surgical specimen did not modify significantly the results. Moreover all patients treated with pneumoperitoneum demonstrated a wide intraperitoneal diffusion of the tracer not observed in gasless patients. Conclusions: The results of this study confirm that pneumoperitoneum may play an important role in the evolution of port site metastasis after laparoscopy for gastrointestinal cancer. Key words: Laparoscopic surgery — Port site metastasis — Abdominal cancer
Neoplastic seeding at the site of introduction of the trocar is a frequent complication of diagnostic and operative laparoscopy for intraabdominal neoplasms [1, 4, 10]. The incidence of such complications has been evaluated as 4% by Correspondence to: E. Cavina
Wexner and Cohen after laparoscopic resection [14] of colorectal cancer. In the authors’ experience, trocar site seeding was observed in four cases (two unsuspected gallbladder cancers after laparoscopic cholecystectomy, two gastrointestinal cancers after laparoscopic staging). Exfoliation and subsequent implantation of free viable surgical cells, through surgical manipulation and desquamation of tumor cells from the serosal surface during extraction of the specimen, are suggested to be the most important factors in neoplasm seeding [3, 9, 13]. These mechanisms cannot explain the fact that not all recurrences have been at the port through which the specimen was retrieved and that in some instances recurrences have been observed after retrieval of the specimen placed in a protective bag. A possible role for the pneumoperitoneum has been postulated [6, 14]. The gas turbulence following escape and automatically insufflation can transport and inplant cells in the access wound and in the abdomen. Moreover, CO2 may facilitate the growth of tumor cells. To evaluate a possible role for pneumoperitoneum in tumor cell dissemination, a scintigraphic model was utilized during laparoscopic cholecystectomy (LC) performed for symptomatic cholecystolithiasis. Materials and methods After giving their informed consent, 30 patients affected by symptomatic cholecystolithiasis were enrolled in the study. Those excluded were premenopausal women and men younger than 50 years old, those with suspected cancer, and those with suspected common bile duct lithiasis. All patients underwent LC: 11 patients (group A) underwent LC using CO2 insufflation (CO2-LC) with extraction of the gallbladder without protective bag; nine patients (group B) underwent CO2-LC with protective bag; ten patients (group C) underwent gasless LC with protective bag.
Technique Groups A and B After insufflating the abdomen using a Veress needle, two 12-mm and two 5-mm trocars were inserted. Laparoscopic cholecystectomy was begun using routine technique.
1295
Injection of 3 ml of labeled RBC in the hepatic fossa cholecystectomy Group A CO2—no bag
Group B CO2— bag
Group C Gasless—bag
2 h after VLC Scintigraphy Fig. 1. Scintigraphic protocol utilized for the study.
In all patients 3 ml of autologous red blood cells (RBCs) labeled with Tc (3 mCi, 111 MBq) was injected in a subserosal site at the level of the hepatic fossa after clippage of the cystic duct and cystic artery. After the injection, cholecystectomy was completed using electrocautery. The gallbladder was extracted without a protective bag in the group A patients. In group B the gallbladder was extracted after the insertion in an endobag.
99m
Group C Patients underwent laparoscopic cholecystectomy using a gasless method: Injection of labeled blood cells was performed with the same technique used in group A and group B. The gallbladder was extracted from the abdomen into an endobag. Scintigraphy was performed 2 h after LC: One front image and one lateral image of abdomen were acquired in all patients (Fig. 1). Abdominal single photon emission computed tomography (SPECT) was performed in 25 cases. The chi-square test was used to verify statistical significance.
Results All cholecystectomies were concluded laparoscopically: Because of technical difficulties in two patients gasless cholecystectomy was converted in gas cholecystectomy insuffling CO2 into the abdomen: These two cases were excluded from the study. Thus 28 cases are eligible for evaluation. At scintigraphy in all patients the gallbladder bed was well visualizable (Fig. 2). Radioactive spots in the area of the umbilical trocar were detected in 10/11 (90%) cases in group A, in 7/9 cases (78%) in group B, and in 2/8 cases (25%) in group C (Fig. 3, Table 1). The scintigraphic evaluation of the sites of insertion of the other trocars revealed a positivity in 12 out of 33 trocar sites in group A, nine of 27 trocars in group B, and one out of 24 trocars in group C. The positivity observed in patients in groups A and B was significantly higher than that observed in group C (p < 0.001). Moreover, all patients treated with pneumoperitoneum (PNP) demonstrated a wide intraperitoneal diffusion of the tracer not observed in gasless patients.
Discussion Metastatic cell seeding is one of the most feared complications following operations of malignancies. Trocar site seeding is frequently reported after laparoscopic operations performed for gastrointestinal cancer [12, 14]. The inci-
dence of such complications has been evaluated to be 4% by Wexner and Cohen after laparoscopic resection of colorectal cancer [14]. LC performed in the presence of unsuspected gallbladder carcinoma is frequently associated with trocar site seeding [2, 3, 7, 13]. In the authors’ experience, 1,500 LCs have been performed: Gallbladder specimens routinely underwent histologic examination and in five cases preoperatively unsuspected carcinoma was found. In two (40%) cases trocar site seeding was observed, respectively, 3 and 5 months after operation. Two other cases of tumor seeding were observed after diagnostic laparoscopy of a case of pancreatic cancer and a case of right colon cancer: In both cases peritoneal metastases were present at laparoscopy. Exfoliation and subsequent implantation of free viable surgical cells through surgical manipulation and desquamation of tumor cells from the serosal surface during extraction of the specimen seems to be the most likely cause of seeding. These mechanisms cannot explain the fact that not all recurrences have been observed at the port through which the specimen was retrieved and that in some instances recurrences have been observed after retrieval of the specimen placed in a protective bag [13]. In these cases, malignant cells can desquamate during the operation: During the manipulation of the resected specimen into the bag, resting on the exterior surface of the bag, these cells could implant themselves while passing through the umbilical trocar site. Another possibility is that after deflation the abdominal wall sags down, allowing the exfoliated tumor cells in the peritoneal fluid to be implanted into the undersurface of the port wound where mesothelial cells are damaged or missing [11]. All this can explain the cases of positivity at the level of umbilical trocar site observed in groups B and C despite the utilization of a cellophane bag, yet it is not able to explain the significantly higher positivity in patients who had gas cholecystectomy compared to patients having gasless cholecystectomy. A possible role for the pneumoperitoneum has been postulated [6, 14]. The gas turbulence following escape and automatic insufflation can transport and implant cells in the access wound and in the abdomen. (Airborne exfoliated tumor cells carried in the carbon dioxide leaking around the trocars, the so-called ‘‘chimney effect,’’ may get trapped in the port wound surfaces, resulting in parietal recurrences.) Using a hamster model, Jones showed that gas laparoscopy can be followed by trocar site implantation; yet this event was never observed after gasless laparoscopy [8]. Hubens, on the contrary, did not observe a significant role for pneumoperitoneum in enhancing the implantation of free intraperitoneal malignant colon cancer cells in rats [5]. In our experience the significantly higher incidence of positive examinations observed both at umbilical and at accessory trocar sites in patients that underwent gas-LC confirms the hypothesis of a possible role of pneumoperitoneum in the dissemination of cells in the abdominal cavity: Aerosolization of labeled red blood cells that get trapped in port wound surfaces is the most likely cause of the high positivity detected in gas-LC. The results of this study—a significantly higher rate of positive examinations in group A and group B despite the utilization of protective bag in group B—suggest an effective, but not exclusive, role of pneumoperitoneum in disseminating labeled RBCs. Similarly, malignant seeding
1296 Table 1. Positivity at scintigraphya
Umbilical site Other sites
Group A
Group B
Group C
10/11 (91%) 12/33 (37%)
7/9 (78%) 9/27 (33%)
2/8 (25%)* 1/24 (4%)*
a
Group A: CO2 pneumoperitoneum: gallbladder extraction without endobag; group B: CO2 pneumoperitoneum: gallbladder extraction with endobag; group C: gasless LC: gallbladder extraction with endobag. * p < 0.001.
trocar seeding can be related to the fact that the surgical trauma and gas facilitate the growth of tumor, creating negative immunological circumstances. In conclusion, we suggest that pneumoperitoneum plays an effective role in aerosolization of RBCs and in their ‘‘implant’’ at the level of port wound surfaces. We believe that, despite multiple mechanisms being involved, pneumoperitoneum may play an important role in the port site recurrences following laparoscopic operations for malignancies.
References
Fig. 2. Scintiscan obtained 2 h after LC in a patient treated with gasless LC shows accumulation of the tracer in the gallbladder fossa at the level of the injection site. Fig. 3. Scintiscan obtained 2 hours after LC in a patient treated with gas-LC shows an accumulation of isotope in the injection site and at the level of umbilicus: Moreover a widespread of the tracer in the abdomen is well evident.
in trocar sites may be the result of aerosilization and forced egress of cells from peritoneum as a result of pneumoperitoneum: The gas turbulence resulting from leaks and reinsufflation episodes may deliver suspended malignant cells to access wounds. Moreover, the role of CO2 in developing
1. Berends FJ, Kazemier G, Bonjer HJ, Lange JF (1994) Subcutaneous metastases after laparoscopic colectomy. Lancet 344: 1994 2. Clair DG, Latz DB, Brooks DC (1993) Rapid development of umbilical metastases after laparoscopic cholecystectomy for unsuspected gallbladder carcinoma. Surgery 113(3): 355–357 3. Copher JC, Rogers JJ, Dalton ML (1995) Trocar site metastasis following laparoscopic cholecystectomy for unsuspected carcinoma of the gallbladder. Case report and review of the literature. Surg Endosc 9: 348–350 4. Fodera M, Pello MJ, Atabek U, Spence RK, Alexander JB, Camishion RC (1995) Trocar site tumor recurrence after laparoscopic assisted colectomy. J Laparoendosc Surg 5(4): 259–262 5. Hubens G, Pauwels M, Hubens A (1995) Laparoscopic insufflation of the abdomen does not increase peritoneal implantation of free intraperitoneal colon cancer cells. Surg Endosc 9: 181 6. Kazemier G, Bonjer HJ, Berends FJ, Lange FJ (1995) Port site metastases after laparoscopic colorectal surgery for cure of malignancy. Br J Surg 82: 1141–1142 7. Jacobi CA, Keller H, Monig S, Said S (1995) Implantation metastases of unsuspected gallbladder carcinoma after laparoscopy. Surg Endosc 9: 351–352 8. Jones DB, Guo IW, Reinhard MK (1995) Impact of pneumoperitoneum trocar site implantation of colon cancer in hamster model. Dis Colon Rectum 38: 1182–1188 9. Lucciarini P, Konigsrainer A, Ebert T, Margreiter R (1993) Tumour inoculation during laparoscopic cholecystectomy (Letter). Lancet 342: 59 10. Nduka CC, Monson JRT, Menzies Gow N, Darzi A (1994) Abdominal wall metastases following laparoscopy. Br J Surg 81: 648–652 11. Ng WT, Yeung HC, Koh GH, Ng WF (1996) Mechanism for port-site metastasis after laparoscopic cancer surgery. Br J Surg 83: 1478–1484 12. Ramos JM, Gupta S, Anthone GJ, Ortega AE, Simons AJ, Beart RW (1994) Laparoscopy and colon cancer: is the port site at risk? A preliminary report. Arch Surg 129: 897–900 13. Saile M, Debus S, Fuchs KH, Thiede A (1995) Peritoneal seeding of gallbladder cancer after laparoscopic cholecystectomy. Surg Endosc 9: 1298–1300 14. Wexner SD, Cohen SM (1995) Port site metastases after laparoscopic colorectal surgery for cure of malignancy. Br J Surg 82: 295–298
