Introduction

Port-site metastasis (PSM) after laparoscopic surgery for colorectal cancer was first reported in 1993 [1], 2 years after the first report of laparoscopic colectomy [2]. In the 1990s, the incidence of PSM was reported to be up to 21 % [3], and the oncological safety of laparoscopic surgery for colorectal cancer was discredited. Curet thoroughly reviewed the literature regarding PSM after laparoscopic surgery in 2004 [4]. However, in recent years, the long-term outcomes of the large, randomized trials comparing open and laparoscopic surgery for colorectal cancer have shown the non-inferiority of laparoscopic surgery for T4 tumors and an actual incidence of PSM around 1 %, not significantly different from the rates of wound recurrence after open colorectal surgery [5–7]. However, although the incidence of PSM after laparoscopic surgery for colorectal cancer has dropped substantially in recent years, it still occurs [8, 9]. Given the widespread application of laparoscopic surgery for advanced colorectal cancer [10], we should update our knowledge regarding PSM.

The rate of performing laparoscopic surgery for gastric cancer has also been rapidly spreading in recent years [11]. The possibility of PSM after laparoscopic surgery for gastric cancer should therefore also be considered. The etiology of PSM is wide-ranging and was closely described in Curet’s review [4]. Animal experiments revealed that pneumoperitoneum plays a role in the exfoliation of cancer cells from the tumor surface into the intraperitoneal gaseous atmosphere by aerosolization. Some of these free cells remain viable and have metastatic potential. PSM is usually considered not a surgical complication but an oncologic outcome [12], and the technical aspects seem to play a greater role than other aspects [13].

We herein reviewed the current knowledge regarding PSM after laparoscopic surgery for colorectal and gastric cancer.

PSM after laparoscopic surgery for colorectal cancer

After Berends reported in 1994 that the incidence of PSM was 21 % (3 of 14 patients) [3, 4] 7 case-reports of PSM after laparoscopic colectomy were published up to 1998 [14]. However, in the 2000s, the rates of reported PSM drastically decreased (Table 1).

Table 1 The historical data on port-site metastases after laparoscopic surgery for colorectal cancer
Full size table

The long-term outcomes of three large, multicenter, prospective, randomized controlled trials, the COST, COLOR, and UK MRC CLASICC trials, were reported in the late 2000s [5–7]. These trials proved the oncologic safety of laparoscopic surgery for colorectal cancer, including the low incidence of PSM (Table 2). The COST trial, in which 428 laparoscopic colectomies versus 435 open colectomies for colorectal cancer were involved, reported a 5-year incidence of PSM of 0.9 % (2 cases) in the laparoscopic arm and 0.5 % (1 case) in the open arm [5]. In the COLOR trial, 7 cases of PSM were reported among 534 cases of laparoscopic colectomies for colon cancer at the 5-year interval, and only 5 of the 7 were “true” PSM, localized on the trocar insertion sites, while the other 2 were extraction minilaparotomy metastases [6]. The UK CLASICC trial compared 526 laparoscopic and 268 open resections for colorectal cancer and reported 9 PSMs in the laparoscopic group at 5 years, only 1 of which was a “true” PSM [7]. In these 3 randomized trials, the rates of T4 tumor in the laparoscopic arms were 3, 6, and 14 %, respectively, which were similar to the open arms.

Table 2 The results of randomized trials comparing open vs. laparoscopic surgery for colorectal cancer
Full size table

After these three large trials, Zanghi et al. conducted a meta-analysis to evaluate and compare the risk of PSM and wound recurrence after laparoscopic colorectal surgery and open surgery for colorectal cancer [15]. Fourteen randomized controlled trials from 1998 to 2010 were included. No significant differences were found between the two groups, not only in the incidence of PSM or wound recurrence, but also in cancer-related mortality during the follow up period of the study. These authors suggested that PSM might be the result of suboptimal surgical techniques and might have occurred in the early phase of the learning curve.

PSM after laparoscopic surgery for gastric cancer

Few reports have been published regarding PSM after laparoscopic surgery for gastric cancer; wound recurrence after open gastrectomy is also extremely rare [16]. Schaeff et al. reported six cases of PSM from gastric cancer, where five of the six patients underwent diagnostic laparoscopy with liver metastasis or peritoneal dissemination [14]. Our group previously reported that subcutaneous port-site metastasis was observed in 2 (1.5 %) of 131 patients who had peritoneal metastasis of gastric cancer and received intraperitoneal chemotherapy through an implanted subcutaneous infusion port [17]. PSM after laparoscopic gastrectomy has rarely been reported since the first case in 2007 [18]. Yoshimura et al. reported no PSM in 209 patients who underwent laparoscopic gastrectomy for advanced gastric cancer [19]. Lee et al. reported that PSM did not occur among 601 patients who underwent laparoscopy-assisted distal gastrectomy [20]. Additionally, Sakurai et al. reported a case of PSM after laparoscopic distal gastrectomy for early gastric cancer [21]. These results may indicate that PSM is less common in gastric cancer than in colorectal cancer, although we should be aware that it can occur even in patients with early-stage gastric cancer. For more accurate incidence of PSM from gastric cancer, we should await the results of ongoing prospective randomized trials [22, 23].

Etiology and prevention of PSM

The etiology of PSM is not completely known, but a number of factors have been implicated. The decrease in the incidence of PSM over time may indicate that the main cause of PSM might be rooted in the technical aspect.

In the early 2000s, Curet reviewed the etiology of PSM and described each suspected cause of PSM as follows: direct implantation, contamination of surgical instruments, aerosolization of tumor cells, chimney effect, surgical technique, excessive manipulation of tumor, pneumoperitoneum, hematogenous spread, and local and systemic effects of carbon dioxide with pneumoperitoneum [4]. In Curet’s review, two main factors were suggested as the cause of PSM: pneumoperitoneum and contamination by inadequate handling of the tumor. Pneumoperitoneum plays a role in the exfoliation of malignant cells from the tumor surface into the intraperitoneal gaseous atmosphere by aerosolization, a some of these free cells remain viable. However, the extent of the influence of pneumoperitoneum remains unclear. Although high pneumoperitoneal pressure increases the rate of tumor cell aerosolization, it has not been proven to increase the rate of PSM. Furthermore, PSM also occurs after thoracoscopy or gasless laparoscopy, during which no CO2 is used [9]. In recent years, no study has investigated the relationship between pneumoperitoneum and PSM.

As for the technical aspects of PSM prevention, Balli et al. pointed out the risks associated with laparoscopic colectomy [13]. In Balli’s review, irrigation of the wound and instruments using Betamine (povidone–iodine) was recommended, based on Neuhous’s 1988 paper [24]. Although Neuhous proved that peritoneal washing with Betamine after colorectal surgery reduced the rate of PSM in a rat model, wound irrigation with povidone (Betamine) is usually no longer done, as it was proven that the routine use of Betamine irrigation was of no benefit and might actually increase the incidence of infection compared with saline wound washing, due to its suppressive effects on local leukocytes and fibroblasts working for wound healing [25]. We have modified Balli’s table on Betamine irrigation (Table 3).

Table 3 The suggested techniques for preventing port-site metastasis after laparoscopic colectomy [13]
Full size table

Conclusions

Current data from large randomized trials show that PSMs are acceptably infrequent in laparoscopic surgery for colorectal cancer. As for gastric cancer, although PSM is extremely rare, we should await the results of large studies. The marked decrease in the rate of PSM over time may suggest that technical aspects may be the biggest cause of PSM, and accordingly, surgeons should make a maximum effort to prevent PSM.