9 Focusing Our Attention on Trocar Seeding!

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Contents

Introduction 221

Recurrence of Port Site Metastasis in Laparoscopic Urology 222 Experimental Studies 223 Discussions 224

Conclusion 226 References 226

Introduction

Over the last decade, modern laparoscopic equipment and techniques have dramatically increased, expand- ing the indications to malignancies [1]. This fact in- troduces a new potential complication: the risk oftumor seeding. Port site recurrences have been reported after laparoscopic surgery to indicate local tumor seeding [2±4]. Implantation has occurred at the Veress needle, laparoscopic trocar port sites and also in the form of peritoneal dissemination [5]. The risk of tumor seeding came from the consolidate experience of laparoscopic procedures in general and gynecological surgery.

The initial descriptions ofport site recurrences were after gynecological procedures for ovarian tumors. The first report dates back to 1978 and con- cerned diagnostic laparoscopy in one patient with carcinomatosis ascites [6]. Afterward an increasing number ofport site metastases in laparoscopy for neoplastic diseases was reported: in 1985 Stockdale et al. for ovarian adenocarcinoma [7], in 1990 Cava et al. for gastric adenocarcinoma [8] and Russi et al. in 1992 for liver carcinoma [9]. Trocar port metastases have been described in the literature after laparoscopic biopsy for hepatocellular carcinoma [9], laparoscopic cholecystectomy for an undiagnosed pancreatic carcinoma [10] and after laparoscopic resection of unsuspected or low malignant ovarian cancer [2]. Johnstone

reported 23 cases ofport site recurrences after thoracoscopic procedures for lung neoplasms [11]. From these series ofreports we realize that both diagnostic or operative laparoscopy can develop tumor seeding.

Laparoscopy has become the most frequently performed operation, as an effective diagnostic tool for evaluation ofacute abdominal gynecological conditions, especially in young women. When suspicious excrescences are detected on the surface of ovarian masses by diagnostic laparoscopy, it is common sense in gynecology to change laparoscopy in exploratory laparotomy and excision ofthe masses. Biopsy should not be performed on these papillary masses during laparoscopy examination. This conservative view is based on an extensive review ofthe literature with evidence ofthe potential oftumor implantation after laparoscopic biopsy made during a diagnostic procedure [3].

Laparoscopic cholecystectomy appears to be the most common and codified procedure in general surgery indications. From a review made on 117,840 patients who underwent laparoscopic cholecystectomy, 409 presented nonapparent gallbladder cancer, with a real incidence of0.35%. In this series, the overall incidence ofport site metastases was 17%. In contrast, data show that wound recurrence following open cholecystectomy for primary nonapparent carcinoma of the gallbladder must be an exceptional event. Paolucci did not find any of these complications in the literature between 1960 and 1997 [4].

The same concern also exists for colorectal surgery.

In 92 laparoscopic resections for colon carcinoma, Fingerhut reported an overall incidence ofport site recurrence of3.2%. Prasad et al. reported a 4% incidence ofport site recurrence in a series of50 patients.

Berends et al. noted three port metastases in 14 patients, corresponding to 21%. Ramos et al. found three wound recurrences, two ofthem with peritoneal carcinomatosis, a 1.4% rate. We believe that the incidence

9 Focusing Our Attention on Trocar Seeding!

Giampaolo Bianchi, Salvatore Micali,

Antonio Celia, Adara Caruso, Guglielmo Breda

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ofthis complication in colorectal laparoscopy is 2.5%, calculated as an average ofthe results achieved from the reports mentioned above. Many other cases oftumor seeding have been described for other indications such as esophageal carcinoma and lung adenocarcinoma [3].

From this review, it seems that there is a specific laparoscopy risk for intraoperative tumor cell seeding and implantation. Moreover, the probability ofdevel- oping abdominal wall metastasis is higher after laparoscopy for cancer than after open surgery.

Recurrence of Port Site Metastasis in Laparoscopic Urology

Since the first nephrectomy performed by Clayman in 1990 (Clayman 1991), there has been considerable growth in laparoscopic urological surgery, slowly at

first and then much more rapidly over the last 5 years with the development ofadrenal gland, kidney and prostate cancer surgery.

The laparoscopic lymphadenectomy (LPLND) in the staging ofprostate cancer was one ofthe first laparoscopic indications in the field of urology. At the same time, the indications for staging lymphadenectomy were extended to transitional cell carcinoma (TCC) ofthe bladder. The first urological tumor seeding reported was during a laparoscopic lymphadenectomy for a bladder tumor, reported by Stolla et al.

[12]. After that in the following 4 years, two tumor seedings were reported after laparoscopic biopsy for bladder TCC and one after staging lymphadenectomy.

Finally, only one case ofprostate cancer seeding was reported after a laparoscopic staging lymphadenectomy [13]. Now we can state that the real incidence after LPLND for prostate cancer is 0.1% and for TCC it is 4% [14]. Tumor seeding during LPLND seems to

Table 1. Trocar tumor seeding after urological laparoscopy in malignancy after lymphadenectomy

Author Year Age

(years) Diagnosis Procedure Time presentation (months)

No. of

implants Follow-up

(months) Stage and grade (G)

Stolla et al. [12] 1994 58 Bladder TCC LL 9 1 Died 9 pT3N0M0/G2

Bangma et al.

[13] 1995 66 Prostatic

carcinoma LL 6 1 Died8 pT3N1M0/G2

Andersen [57] 1995 61 Bladder TCC LB ± 1 Died 12 pT3N1M0

Elbahnasy [14] 1998 63 Bladder TCC LL 3.5 1 Died 3 pT3N1M0/G2

C carcinomatosis, LL laparoscopic lymphadenectomy, LB laparoscopic biopsy

Table 2. Trocar tumor seeding after urological laparoscopy in malignancy after radical nephrectomy and nephroureterectomy

Author Year Age

(years) Diagnosis Procedure Time presentation (months)

No. of

implants Follow-up

(months) Stage and grade (G)

Shaikh et al. [27]1998 66 TCC upper

tract LNU 8 1 ± pT2N0M0/G?

Barret andFan-

tie [23] 1999 76 RCC LN 25 1 ± PT3N0M0/G4

Otani et al. [28] 1999 74 TCC upper

tract LNU 3 1 ± pT2N0M0/G?

Landman and

Clayman [25] 2001 72 RCC LN 5 multiple Died8 pT1N0M0/G2^a

Landman and

Clayman [25] 2001 32 RCC LN 12 1 ± pT1N0M0/G2^a

LN laparoscopic nephrectomy, LNU laparoscopic nephroureterectomy

aFuhrman grade

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be much more common for bladder TCC than for other urinary tract malignancies because TCC is more aggressive than other urological tumors (Table 1).

With the exception oflaparoscopic lymphadenectomy as mentioned before, laparoscopic urological surgery in the beginning was dedicated mostly to treating benign disease such as simple nephrectomy. The first two reports describing laparoscopic radical nephrectomy for renal cell carcinoma (RCC) were published in 1993 and a total offive cases were reported [15, 16]. Subsequently, most centers throughout the world started radical laparoscopic nephrectomy and results from a bigger series state the feasibility and reproduc- ibility ofthis procedure [17±19]. The same occurred for laparoscopic nephroureterectomy (NU); the first case report was performed in 1991 at Washington Uni- versity [20]. Since then several limited series have been reported, demonstrating the safety and efficacy ofthe procedure [22, 23]. The use ofthese minimally invasive techniques with or without morcellation for specimen extraction is associated with potential port site metastasis (Table 2).

In 1999, Barret and Fantie reported a laparoscopic nephrectomy in a patient with T3N0M0 grade IV RCC and a 862-g pathological specimen who had a solitary port site recurrence at 25 months offollow-up. The specimen was entrapped in the Cook LapSac and frag- mented with the Cook electrical mechanical morcellation tool [24]. Castilho et al. reported a case ofab- dominal wall metastases following laparoscopic radical nephrectomy for a clinical stage T1N0M0 renal cell carcinoma. The specimen was retrieved en bloc by mechanical morcellation in an intact plastic bag [25].

Afterwards Castilho reported another case of port site tumor recurrence in a 32-year-old woman with a right renal mass of4 cm 12 months after surgery. Laparo- scopic radical nephrectomy was performed without complications and the pathological study revealed low Fuhrman grade 2 renal cell carcinoma.

The efficacy of laparoscopic radical nephroureterectomy for upper-tract TCC has been well documented [26]. Up to 1998, the literature did not report any tumor seeding or port site metastasis despite morcellation ofsome the nephroureterectomy specimens within an impermeable entrapment sack. In 1998, Shaikh et al. reported the first case of port site recurrence after laparoscopic nephroureterectomy 8 months after the surgery [27]. Then Otani reported a second case ofport site metastasis following laparoscopic nephrectomy for tuberculous atrophic kidney and unsus-

pected TCC 3 months after surgery [28]. The last trocar tumor seeding reported in the urological literature was after a lymphadenectomy for retroperitoneal metastases ofan epidermoid carcinoma ofthe testis [29].

Experimental Studies

What are the mechanisms involved in trocar site recurrences?

Recent studies review the current knowledge on laparoscopic mechanisms ofcancer dissemination and addresses to experimental models ofcancer dissemination in animals [30]. Several authors have investigated the neoplastic cells pre-existing in the peritoneum, the increased exfoliation of tumor cells result- ing from greater manipulation near the tumor or at the tumor itselfby laparoscopic instruments as possi- ble causes ofwound implantation [31, 32]. Recently, Juhl et al., using immunocytological methods, found neoplastic cells in the peritoneal cavity in 27% ofthe patients with colorectal tumors, 43% ofpatients with gastric cancer and 58% of the patients suffering from pancreatic cancer [33]. Some authors have investigated the local factors and specific factors that allow neoplastic cell adhesion and the growth at the trocar site (Table 3).

The first mechanism studies is the aerosol ability ofthe pneumoperitoneum and several in vitro models are contradictory. Whelan et al. recovered no free mel- anoma cells injected into the abdominal cavity under pressurized CO2 in the abdomen [34]. In contrast, Knolmayer et al. reported recovery ofexfoliated peritoneal cells after various levels of intra-abdominal

Table 3. Specific factors connectedwith laparoscopic surgery Laparoscopic instruments

Exfoliation andadhesion to laparoscopic instruments Trocar cannulas

Local wound adhesion and seeding of neoplastic cells locatedin the cannula surface

Neoplastic tissue retrieval Tight andnarrow port site Pneumoperitoneum

Closedsystem with an increasedconcentration of neoplastic cells gaseous turbulence, chimney effect along trocar cannulas, modification of tumor cell biology by CO2

Facilitation of cell adhesion by wound factors (fibroblast, collagen, proteoglycans, platelets)

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pressurized carbon dioxide [35]. Other authors sug- gested that smoke particles can act as carriers of clumps ofneoplastic cells and can be recovered when exhaled by the trocar orifices due the high intra-abdominal pressure [36]. This finding could explain the implant at trocar sites.

Other authors have studied intra-abdominal cell ki- netics after injection of free cells in the abdominal cavity during laparoscopy or open surgery. In an in vivo porcine model, after the filtered exhaust of the trocars only in one case tumor cells was found. More importantly, cells were recovered in 20% oftrocar and 40% ofinstruments [37]. The introduction ofgasless laparoscopic surgery seems to be an important factor in establishing the role ofpneumoperitoneum as a vector oftumor seeding. Watson et al. observed a reduction in port site metastases, from 83% to 25%, respectively, with gasless or CO2 laparoscopy after manipulation oftumor ofthe abdominal wall induced with injection ofbreast cancer cells [38]. Other studies have been designed to observe the pattern oflate dissemination ofcancer cells after inoculation in the abdomen. Tsuvian et al. did not find a different pattern ofdissemination after intra-abdominal RENCA cell inoculation: there were similar growth rates and implants, and finally he stated that the pneumoperitoneum does not facilitate port site metastases [39].

The ability oftumor cells to adhere to the intact or disrupted peritoneum was tested. Using bladder cancer cells in a mouse model, these authors showed that after instillation of tumor cells in the abdomen with an intact or injured peritoneum, the carcinomatosis rates were 50% and 63%, respectively; but ifheparin was added simultaneously the presence ofimplants fell to 17% and 31%, respectively. These experimental studies in animal models evaluated the implant of heparin and the pentapeptide Gly-Arg-Gly-Asp-Ser (GRGDS) and TCC inoculated in the peritoneal cavity, with prevention oftumor implantation [40]. Recently, Lewis et al. demonstrated the therapeutic potential use ofCopper-64-pyruvaldehyde-bis(N(4)-methylthiosemicarbazone) in inhibiting cancer cell implantation and growth at doses well below the maximum tolerated dose, with no signs oftoxicity to hamsters [41]. This washing trick seems to achieve the target ofreducing the possibility oftumor implantation. Other authors reported the effect of intraperitoneal irrigation with taurolidine and octreotide on port site and liver metastasis after staging laparoscopy in a chemically induced pancreatic adenocarcinoma. The number of

liver metastases per animal was increased after saline irrigation compared to taurolidine or octreotide. Port site metastases were found in 36.8% after saline, in 37% after octreotide and 0% after taurolidine irrigation [42].

From experimental studies, it appears that a laparoscopic approach has potential advantages and disad- vantages. In a recent review ofexperimental studies, Canis et al. affirmed that the risk of dissemination appears high when a large number ofmalignant cells are present in peritoneum and adnexal tumors with exter- nal vegetations, and bulky lymph nodes should be considered as contraindications to CO2 laparoscopy.

Depending on the model used, controversial results have been reported on the incidence oftrocar site metastasis when comparing CO2 laparoscopy and laparotomy [43]. We believe that more experimental study is necessary to consolidate the effective risk of tumor seeding during laparoscopy.

Discussions

Reports oftumor implantation after laparoscopic procedures in patients with intra-abdominal malignancies are a source ofincreasing concern and the most important factor precluding widespread employment of laparoscopy in the treatment ofmalignant disease. In general surgery and gynecology, some reports con- cluded that laparoscopic surgery should not be performed when cancer is suspected, but in controlled studies until there are sufficient data on the clinical importance ofthis complication [44]. The radical na- ture ofthe procedure is not crucial for the risk oftumor seeding. Gynecologists were the first reporting tumor seeding after laparoscopic biopsy of ovarian carcinoma. It is common sense among gynecologists to convert to open surgery when suspicious excrescences are detected on the surface of ovarian masses during diagnostic laparoscopy. No biopsy should be performed on these papillary masses during laparoscopic examination. This conservative view is based on an extensive review ofthe literature with clear evidence oftumor implantation after laparoscopic ovarian biopsy [3]. Other case reports from general surgery describe port site metastasis after diagnostic laparoscopy for gastric adenocarcinoma, liver carcinoma and pancreatic carcinoma [8±11]. The real mechanism oftumor seeding during diagnostic laparoscopy is not clearly understood, but probably it is related to tumor

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cell exfoliation at the biopsy site. This situation can be worse ifthe tumor is very aggressive.

In laparoscopic colorectal surgery, reports on tumor implantation and portal seeding are fairly discordant.

As a result ofreviews in colorectal oncology, the per- centage oftumor seeding ranged from 3.2% to 21%

[13±15]. At the same time, the overall incidence ofport site metastases after laparoscopic cholecystectomy for gallbladder cancer is 14%±30% [45]. In an effort to ob- tain more knowledge on the impact ofsurgical technique on the prognosis ofgallbladder cancer, in 1997 the Surgical Endoscopy Working Group ofthe German Society ofSurgery started a registry ofall cases ofcho- lecystectomy, laparoscopic as well as open, with a post- operative incidental finding of gallbladder carcinoma.

Results will be available in 5 more years [45].

The laparoscopic benign cholecystectomy appears the most common and codified procedure in general surgery indications. From a recent survey on 117,840 cases, was reported an incidence of0.35% ofnonap- parent gallbladder cancer, and in this series the overall incidence ofport site metastases is 17%. In contrast, data show that wound recurrence following open cholecystectomy with primary nonapparent carcinoma of the gallbladder must be an exceptional event. Paolucci did not find any of these complications in literature between 1960 and 1997 [4]. It is clear that laparoscopy makes the difference, but the actual cause is still not well understood. The last decade witnessed major shifts in popularity of laparoscopic procedures for the therapy ofurological disease. The pioneering work of Ralph V. Clayman in 1990 prompted an explosion of interest in laparoscopic techniques, which was soon tempered by the realization that the benefits attributed to laparoscopic procedures vs open surgery [46] had to be offset by the disproportionate time and financial investments required for the acquisition of technical skills, their maintenance and upgrading. A second change ofthe winds has occurred in the last few years, after the demonstration that such techniques could safely be used in the therapy of neoplastic disease ofthe kidney and the prostate. These days laparoscopic surgery as therapy for urological oncology can be roughly divided in three main categories:

widely accepted, controversial and experimental. Re- viewing the laparoscopic urological literature, the main oncological indications are renal, adrenal and prostate cancers.

Laparoscopic urological surgery in malignancy pre- sents tumor seeding complications as well as in gener-

al and gynecological surgery. The first tumor seeding reports were described after five laparoscopic lymphadenectomy or nodal biopsy for four bladder cancer patients and one prostate cancer patient. Moreover, all were advanced cancer, none used entrapment sac and all were isolated case reports. Four offive were TCCs, considered an extremely aggressive tumor. Kavoussi et al. reviewed 372 cases ofLPLND in patients with prostate cancer, and in this survey there were no cases oftumor seeding [47]. Moreover, Vallancien et al. performed 813 laparoscopic radical prostatectomies and 177 LPLNDs and reported no tumor seeding [1]. What is particularly disconcerting is that there are already four reports of metastases after laparoscopic diagnostic procedures for bladder TCCs, but large series of LPLND for bladder cancer are not reported in prostate cancer [14].

Laparoscopic radical nephrectomy is considered safe and oncologically appropriate for patients with RCC [48]. To date, laparoscopic surgery for localized RCC has not been associated with an increased risk of port site, intra-abdominal or retroperitoneal recurrences or metastatic disease [17±19, 49]. TCC ofthe upper urinary tract represents 5% ofall urothelial tumors and 5%±10% ofrenal tumors [50]. Complete re- moval ofthe upper urinary tract with a bladder cuff requires exposure ofthe retroperitoneum adjacent to the kidney, ureter and bladder. It is well known that laparoscopic NU is a less invasive alternative to open NU and the principles ofsurgical oncology can be maintained [26, 51]. A total offive tumor seeding metastases secondary to renal cancer (three RCCs and two TCCs) are reported. In four cases Endobags were used for specimen extraction. In only one case of NU was the specimen removed intact through a small transverse incision by extending one ofthe ports later- ally. All RCC specimens were morcellated inside a LapSac and removed through one ofthe trocars (Ta- ble 4). All these reports seem pertinent with oncological asepsis, but a few comments should be highlighted.

Barret and Fantie operated on a large specimen that weighed 862 g, an aggressive Fuhrman grade IV/IV and sarcomatoid elements. In one oftwo cases, Castil- ho et al. reported the presence ofascites, which can be a cause oftumor cell dissemination [2]. The other case was performed with strict adherence to oncological principles. Considering that TCC is the most aggressive renal cancer, the specimen should be placed in an entrapment sac, a condition that was not re- spected by Ahmed et al. Tumor seeding reported by

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Otani et al. occurred from an unsuspected TCC, because the patient underwent a simple nephrectomy for tuberculous atrophic kidney.

The last trocar tumor seeding reported in the urological literature describes a case report ofa lymphadenectomy to treat retroperitoneal metastases ofan epidermoid carcinoma. Sebe et al. describe extraction ofthe kidney inside a entrapment sac, but how lymph an nodes were extracted was not described.

Many experimental studies have been designed to understand the risks oflaparoscopic surgery in cancer. Regarding surgical access, controversial results have been published in solid tumor models, and trocar site metastases were significantly more common after laparoscopy [52, 53]. After an intraoperative injection ofcells, two studies showed a higher incidence ofwound metastases after laparotomy [54, 55]. In animal models, the effect of CO2 pneumoperitoneum seems to have correlation with the volume ofcells injected, but high pressure ofCO2 insufflation does not increase the risk ofimplantation ofmalignant cells [56]. Experimental studies have documented very well that traumatic handling ofthe tumor and trauma to the trocar site increases the incidence ofport site metastases [32, 33]. Taurolidine with or without heparin seems very important in order to decrease the number and the volume ofperitoneal metastases [41, 42].

Further experimental studies should be conducted to evaluate the risk oftumor dissemination. By now a few clear-cut rules appear mandatory: remove the whole specimen inside an entrapment sac and without morcellation, avoid trauma to the trocar site, avoid gas leakage around the trocar, select the case (no advanced and aggressive cancer), minimize tumor manipulation.

Conclusion

Port site metastases are secondary to a number offac- tors, including the technical skill ofthe surgeon's no touch technique, biological properties ofthe tumor, and local environmental aspects. Undoubtedly, laparoscopy can favor dissemination of aggressive tumors.

The use ofa plastic bag for specimen retrieval is a logical method to avoid contact between malignant tissue and peritoneum or skin. This measure must be considered mandatory for extraction of suspected or assessed cancer tissue, assuming that this precaution does not exclude an intraperitoneal or trocar site recurrence.

Tumor seeding following laparoscopic surgery in malignancies seems a minor concern in urology compared to gynecology and general surgery. The reasons are not clearly understood, but they are possibly related to different tumors' biological properties and anatomy. Further research is warranted in this field.

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Table 4. Use of Endobag and morcellation in renal cancer

Author Cancer Endobag Morcellation

Barret andFantie

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Landman and

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Landman and

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9 Focusing Our Attention on Trocar Seeding!

Introduction

9 Focusing Our Attention on Trocar Seeding!

Recurrence of Port Site Metastasis in Laparoscopic Urology

Experimental Studies

Discussions

Conclusion

References

10 Complicated Cases