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Evaluation of single-port laparoscopy for peritoneal carcinomatosis assessment in advanced ovarian cancer
European Journal of Obstetrics & Gynecology and Reproductive Biology 181 (2014) 60–65
Contents lists available at ScienceDirect
European Journal of Obstetrics & Gynecology and Reproductive Biology journal homepage: www.elsevier.com/locate/ejogrb
Evaluation of single-port laparoscopy for peritoneal carcinomatosis assessment in advanced ovarian cancer Delphine Quaranta *, Eric Lambaudie, Mellie Heinnemann, Gilles Houvenaeghel, Elisabeth Che´reau Department of General and Oncological Surgery, Paoli Calmettes Institute, 232 Boulevard Sainte-Marguerite, 13273 Marseille, France
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 January 2014 Received in revised form 4 July 2014 Accepted 20 July 2014
Objectives: Ovarian cancers are usually diagnosed at an advanced stage. The extent of the disease before surgery partly determines the ability to perform a complete cytoreduction. The peritoneal cancer index (PCI) is used to evaluate peritoneal carcinomatosis and has been validated in ovarian cancer and correlated with resectability. The aim of our study was to assess the feasibility of single-port laparoscopy (SPL) for suspicion of advanced ovarian cancer and to describe the ability to calculate the PCI score at the time of laparoscopy. Study design: Between February 2011 and January 2013, 33 patients underwent SPL for suspected advanced ovarian cancer. Individual records for all patients were prospectively reviewed and analyzed. For each patient, we determined the PCI score. Results: 33 patients underwent initial SPL, 85% had increased carcinological markers and 67% a radiological suspicion of peritoneal carcinomatosis. The median operative time was 90 min. During SPL, 76% of patients underwent ascites evacuation; all patients had peritoneal cytology and peritoneal biopsies. Only 3 patients experienced perioperative complications. Two open conversions were recorded. Quotation of the PCI score was possible for all patients. Eighteen patients (55%) had a PCI score below 10; one had a maximal PCI score of 39. The PCI score was null for 9 patients. Non-browsing areas marked 8 procedures. Conclusions: SPL appeared to be feasible, with satisfying immediate results and postoperative outcome, compared to conventional laparoscopy. It allowed a satisfying exploration of the abdomino-pelvic cavity and a good description of peritoneal carcinomatosis with only a few non-browsing PCI areas. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Single-port laparoscopy Peritoneal carcinomatosis PCI score Advanced ovarian cancer
Introduction Ovarian cancers are usually diagnosed at an advanced stage, with massive, widespread intra-abdominal disease. Multiple studies reported that the completeness of the primary cytoreductive surgery independently influences survival for these patients [1,2]. Median and five-year survivals after removal of all visible disease (complete cytoreduction) were reported to exceed survival rates resulting from suboptimal procedures (residual disease 1 cm)[2]. The extent of the disease before surgery partly determines the ability to perform a complete
* Corresponding author at: Universitary hospital Archet2, Department of Gynecology and Obstetrics, 151 Route de saint-antoine de ginestiere, 06200 Nice, France. Tel.: +00 33 4 91 22 35 32; fax: +00 33 4 91 22 36 13. E-mail address: [email protected] (D. Quaranta). http://dx.doi.org/10.1016/j.ejogrb.2014.07.008 0301-2115/ß 2014 Elsevier Ireland Ltd. All rights reserved.
cytoreduction. The ability to predict complete resection at the time of diagnosis could be suggested during the preoperative course with a clinical examination, a CA125 level check or radiological examinations. However, it has been demonstrated that these data were insufficient to predict with precision resectability [3]. To quantify with more precision the intra-abdominal extent of the disease, a number of numerical ranking systems have been proposed and could be used during the first step of surgery. The most described was the peritoneal cancer index (PCI), used to evaluate the peritoneal spread in malignant intraperitoneal and pelvic tumors [4,5]. Its use for ovarian cancer has also been reported and its correlation with resectability has been demonstrated in advanced ovarian cancer [6,7]. The performance of a laparoscopy to determine resectability has been demonstrated for advanced ovarian cancer and specific scores were proposed [8–12]. However, some studies underlined the possibility of post site metastasis. In this setting, the use of a
D. Quaranta et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 181 (2014) 60–65
single port could allow a better exploration and description of peritoneal carcinomatosis (2 to 3 instruments in addition to a camera), no additional scar and a larger biopsy for diagnosis. To date, to our knowledge, no study has reported the exploration of peritoneal carcinomatosis using a single-port approach. The aim of this study was to assess the feasibility of a singleport exploratory laparoscopy for suspected advanced ovarian cancer and to describe the ability to calculate the PCI score at the time of the laparoscopy. Materials and methods Patient population Between February 2011 and January 2013, 33 consecutive patients underwent a laparoscopy for suspected advanced ovarian cancer in Paoli-Calmettes Institute, Marseille, France. Individual records for all patients were prospectively analyzed: patient and tumor characteristics, per-operative findings and postoperative course. For each patient, we determined the PCI score. Peritoneal cancer index (PCI) Sugarbaker first described the PCI for colon cancer in 1995 [4]. A few years later, Tentes et al. evaluated the PCI for ovarian cancer [6]. The PCI quantitatively combines the distribution of the tumor throughout 13 abdomino-pelvic regions with a lesion size (LS) score. Lines define nine regions, which are numbered in a clockwise direction, with zero at the umbilicus and one defining the space beneath the right hemidiaphragm. Regions 9 to 12 divide the small bowel into upper and lower jejunum and upper and lower ileum. Each region is also defined by the anatomic structures found there. The LS score is determined after complete lysis of all adhesions. LS-0 means no visible tumor; LS-1 indicates implants less than 0.5 cm in size, LS-2 between 0.5 and 5 cm, and LS-3 greater than 5 cm. This refers to the largest diameter of tumor implants. If there is a confluence of disease matting abdominal or pelvic structures together, this is automatically scored as LS-3. The LS are then summed for all abdomino-pelvic regions. A numerical score from 0 to 39 indicates the extent of the disease within all regions. In the report by Tentes et al. [6], there was a significant difference in the five-year survival rates between patients with a PCI > 10 and 10. A previous study demonstrated the ability of the PCI to predict resectability, post-operative morbidity and outcome in advanced ovarian cancer [7].
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average BMI was 24 Kg/m2 (range: 17–42). Seventy-five percent of the patients had a history of abdominal surgery and six patients had previous cancer history (Table 1). In 76% of cases (n = 25), SPL was performed for clinical or radiological ascites. For 28 of the 33 patients (85%), SPL was motivated by an increase of carcinological markers, and for 22 of patients (67%), by radiological suspicion of peritoneal carcinomatosis (Table 2). The median operative time, from initial umbilical section to last skin stitch, was 90 min (range: 30–188 min). Surgical characteristics are reported in Table 3. During SPL, 25 patients (76%) underwent ascites evacuation. Peritoneal cytology and peritoneal biopsies were performed for all patients. In a few cases, surgical resections were made (4 oophorectomies and 1 salpingectomy). One patient had a bacteriological study of a thickened and purulent peritoneal fluid. Three patients experienced perioperative complications: two small-bowel injuries and one bladder injury. Two open conversions were recorded because of exploration difficulties (adhesions or small bowel injuries). No perioperative transfusion and no major complication occurred. The median hospital stay was 1.84 days (range: 0–12 days). Quotation of the PCI score was possible for all patients (Table 4). Eighteen patients (55%) had a PCI score below 10, one patient had a maximal PCI score of 39 (Fig. 2). The PCI score was null for nine patients. Non-browsing areas marked eight procedures (24%). Three patients had two or more than two non-browsing areas: one for malignant lymphoma and two patients because of major extensive carcinomatosis (Table 5). Region 6, corresponding to the pelvic area, could not be explored in six patients because of blinded pelvis and adhesions. This observation’s failure was noticed in 2 cases for the region ‘‘left lower’’ (region 5) and also for each of the following regions ‘‘right upper’’ (region 1), ‘‘left upper’’ (region 3), ‘‘right lower’’ (region 7), ‘‘upper jejunum’’ (region 9) and ‘‘lower jejunum’’ (region 10) [4]. Comments
The patient was placed in the dorsal decubitus position, and one 3-cm incision was performed across the umbilicus and the single port was installed. As reported previously for extraperitoneal para-aortic lymphadenectomy, we used a single port GelPOINT1 device (Applied Medical) (Fig. 1) [13]. The peritoneal cavity was inflated with carbon dioxide up to a maximum pressure of 10 mmHg. We used a 10 mm laparoscope and 5 mm standard instruments, including fenestrated forceps, bipolar forceps, and monopolar scissors if necessary. No additional trocar was used.
A single-port laparoscopic approach has been recently developed and evaluated. As already reported, it appeared to be feasible, with a satisfying immediate result and post-operative outcome, compared to conventional laparoscopy [13]. It also allowed a reliable evaluation of peritoneal carcinomatosis of our 33 patients, even though 76% of them had undergone previous abdominal surgery. In our study, for 76% of the patients the PCI score has been calculated without missing an area. A median operative time of 90 min, limited hospital stay and absence of major complications also highlighted its interest. Indeed, before surgery, the ability to perform a complete primary cytoreduction is influenced by the extent of disease. Multiple studies have reported that residual disease after surgery was the best predictive factor for survival [2]. In the aim to select patients eligible for complete surgery, surgeons need the tools to establish the precise extent of the disease. In this setting, the FIGO classification is insufficient. Consequently, more detailed quotation systems are necessary at the time of surgery. One previous study has compared the ability of various carcinomatosis scores to predict the extent of the disease in relation to resectability. In this study, PCI and Fagotti modified scores were the most pertinent [1,7]. They outperformed Fagotti and Eisenkop scores [11,14].
Results
PCI score
Thirty-three patients underwent an initial single-port laparoscopy (SPL) in the context of suspected advanced ovarian cancer. The median age of the patients was 62 years (range: 32–84). The
The PCI score gives valuable information about the precise distribution of seeding and tumor volume, representing in detail the peritoneal extent [15]. For ovarian cancer, Tentes et al. reported
Surgical management
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D. Quaranta et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 181 (2014) 60–65
Fig. 1. GelPOINT1, device and installation steps.
that the mean survival and five-year survival rate for patients with a PCI 10 were 80 12 months and 65%, respectively, while the mean survival and five-year survival rate for patients with a PCI > 10 were 38 7 months and 29%, respectively [5]. The PCI score was correlated with survival (p = 0.0253) in their study. Other studies found that a score superior to 10 compromised the ability of optimal surgical management without carcinomatous residue [4,16–19].
Nevertheless, there are some limitations for the use of the PCI score. First, the PCI score might be misevaluated by the existence of non-invasive malignant tumors, such as peritoneal pseudomyxoma, grade 1 sarcoma, and some peritoneal mesothelioma, which could be completely resected. So, a high PCI score might be reduced to a null score after cytoreduction, which means that prognosis does not have to be based on the PCI score only. Secondly, the
D. Quaranta et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 181 (2014) 60–65 Table 1 Patients characteristics. Patients characteristics
n (%), [range]
Age (years) BMI (kg/m2) Previous surgical history -Laparoscopy -Laparotomy -Caesarean Previous neoplasic diseases -Breast -Kidney -Cardia -Endometrial -Ovary
62 [32–84] 24 [17.4–42.55]
the large amount of patients with a previous history of surgery, this result could be considered satisfactory. This rate is below the rate described by Garofalo, but in our study, patients with nonresectable disease underwent neo-adjuvant chemotherapy [21]. The aim of the laparoscopy was to perform a diagnosis biopsy and to conduct exploration to determine resectability with minimal adhesiolysis and morbidity.
18 (54%) 5/33 (15%) 4/33 (12%) 6/33 (18%) 2/33 (6%) 1/33 (3%) 1/33 (3%) 1/33 (3%) 1/33 (3%)
Single-port laparoscopy
Table 2 Indications of laparoscopy. Laparoscopy indication
n
%
Ascites clinic/radiologic Ovarian/pelvic mass on radiological exams Increase of carcinologic markers CA 15.3 CA 125 SCC ACE Ca 19.9 Radiological suspicion of peritoneal carcinomatosis
25 24 6 24 2 2 1 22
76 72 18 73 6 6 3 67
Table 3 Surgical characteristics. Surgical characteristics
n
Operative time (min) Per operative actions Ascites evacuation
0 <500 cm3 500 cm3
Adhesiolysis Peritoneal cytology Peritoneal bacteriology Peritoneal biopsies -Without visible lesions -Supra-millimeter lesions -Infra-millimeter lesions Epiploon systematically suspicious epiploon Sigmoid lesion Rectal lesion Gastric lesion Biopsy of ovarian tumor Surgical resection -Annexectomy -Salpingectomy Per operative complications Per operative transfusions injuries -Small bowel injury -Bladder injury Open conversion to laparotomy Length of hospitalization (days, range)
3 7 25 3 8
5 4 1 0 3 2 1 2 1.84
63
Range (%) 90
30–188
8 11 14 6 33 1
24% 33% 42% 18% 100% 3%
9% 21% 76% 9% 24% 2 3 1 1 15% 12% 3% 5 0% 9% 6% 3% 6% 1–12
6% 9% 3% 3%
15%
Table 4 Peritoneal carcinomatosis index (PCI). PCI score
10
11–20
21–30
31–39
Number of patients (%)
18 (54%)
4 (12%)
10 (30%)
1 (3%)
invasion of some anatomic regions, such as hepatic pedicle with the common bile duct, are inoperable and compromises the prognosis, even though the PCI score is low [20]. In our study, only in 24% of patients did we fail to calculate the exact PCI score because of non-browsing areas. Taking into account
The fundamental interest of SPL lies in having one single incision for all laparoscopic instruments. However, the major drawback with SPL is the absence of ‘‘triangulation’’ which could be technically difficult for laparoscopic surgeons. Each pharmaceutical industry has adopted its own nomenclature for this procedure. The procedure is usually named laparo-endoscopic single-site surgery (LESS) [22]. The Triport (Advanced Surgical Concepts, Wicklow, Ireland), also called R-Port, is a device designed to be used through a unique incision, typically across the umbilicus, because of the fascial defect. This device has been approved by the Food and Drug Administration (FDA). In gynaecology, the first example of SPL was tubal ligation by Wheeless [23]. A single-port laparoscopic hysterectomy with bilateral salpingo-oophrectomy has been reported by Pelosi [24]. GelPOINT1 SPL has been recently described in the Paoli-Calmettes Institute in different surgical indications, such as adnexal procedures or extraperitoneal para-aortic lymphadenectomy [13,25,26]. To our knowledge, no study has reported the use of SPL for the evaluation of resectability in advanced ovarian cancer. To install the GelPOINT SPL an aneurotic incision of 2–3 cm is needed. The peritoneal surface of the shaft contains an autoexpendable ring, which allows a sealing, whatever the thickness of the abdominal wall. The external part of the GelPOINT1 contains three triangular ports incorporated in a gelatinous material, and an opening dedicated to insufflation and maintenance of pneumoperitoneum. The concept of ‘‘triangulation’’ is the main principle of singleport surgery. It allows a good overview and an ergonomic position for the surgeon and his assistants. Hence, the umbilicus appeared to be the most appropriate site for the device. The Triport presents many advantages. First, there is a cosmetic advantage: several instruments of variable sizes could be introduced by one unique incision, through the GelPOINT’s three trocars, without losing pneumoperitoneum. Secondly, there is a carcinologic advantage: in the case of disseminated peritoneal carcinomatosis, the unique incision allows a histological diagnosis and limits the classical carcinomatous dissemination through the site ports [27]. Indeed, port-site dissemination has been described in observations of conventional laparoscopy and removal of the port sites during debulking surgery in advanced ovarian cancer is recommended. Moreover, Alexis spacer, included in the GelPOINT device, is used as a abdominal wall protector. The third advantage is technical: the GelPOINT1 device is easily introduced and removed. The thickness of the abdominal wall is not an obstacle for single-port use. The last advantage highlights the lower morbidity of SPL, compared to conventional laparoscopy: it decreases perioperative complications (vascular, digestive and adjacent organ injuries), post-operative complications (less incidences of hernia, and better cosmetic results) and length of hospital stay [13,28]. The single port might also limit post-operative pain, as suggested in a systematic review [29]. However, the preference for umbilical positioning might be an obstacle when targeted tissue is located too far from the instruments’ articulation. Moreover, it could be difficult to introduce GelPOINT1 SPL elsewhere other than through an abdominal defect.
D. Quaranta et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 181 (2014) 60–65
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Fig. 2. Pictures of peritoneal carcinomatosis.
Table 5 Non-browsing areas. Patients Patient Patient Patient Patient Patient Patient Patient Patient
2 5 12 14 17 21 23 30
Non-browsing areas
Characteristics
Areas 5 and 6 Area 1 Area 3 Areas 5, 6 and 7 Area 6 Areas 6, 9 and 10 Area 6 Area 6
Blinded pelvis-lymphoma Post-operative adhesions Non visible left hemi-diaphragm-carcinomatosis Blinded pelvis-carcinomatosis/adhesions Blinded pelvis-carcinomatosis/adhesions Extensive carcinomatosis Adhesions Adhesions
Because of the ‘‘triangulation’’, manipulation of the camera might cause the involuntary movement of the adjacent instruments. This could increase the difficulties in achieving easy tasks [30]. Using a single-port trocar enforces a restricted external area for the surgeon’s hands, compared to a standard laparoscopy. Indeed, the instruments and the laparoscope are in competition through a unique opening, both on the outside (conflict between hands) and on the inside (conflict of the instruments’ extremity). So, it is essential to develop and distribute empowered instruments that
provide: good articulation, variable sizes, and remote-articulated handles from the entrance trocar, as well as low-profile cameras with Wi-Fi optics. The insufflation tube has to be positioned so as not to interfere with the other instruments. All these measures would free external space and limit collisions. In conventional laparoscopy, a switch of instruments or camera in different ports avoids bad exposure. In SPL, this adaptation is impossible, threatening operative exposure and consequently safety. Using flexible instruments and angular optics could improve exposure and reduce the problem of non-browsing areas.
D. Quaranta et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 181 (2014) 60–65
Exploration of region 3 ‘‘left upper’’, which contains the splenic area, could be more precise with the use of a 308 angular optics, for example. Recently a new technique for assessing the extent of peritoneal carcinomatosis was described, combining manual palpation and standard laparoscopy. Hand-assisted laparoscopy may perform better than laparoscopy alone for predicting the resectability of peritoneal carcinomatosis by increasing the number of sites evaluated [31]. SPL with a unique incision is a new, attractive technology, of interest to investors, surgeons and patients. As reported in our study, this procedure allows the diagnosis of neoplasic disease by enabling samplings such as peritoneal cytology, biopsy. More particularly, its feasibility relies in the calcul of PCI score, allowing a satisfying exploration of the abdomino-pelvic cavity. The precision of SPL is influenced by the surgeon’s experience and a precise knowledge of the PCI score. Ideally, a unique experienced operator should manage the initial laparoscopy with the PCI evaluation and debulking surgery. Conflict of interest statement All authors declare no conflict of interest. Condensation The peritoneal cancer index is validated for laparotomic evaluation of peritoneal carcinomatosis in ovarian cancer. We have assessed the advantages and feasibility of single-port laparoscopy. Acknowledgement The authors thank the staff of Paoli Calmettes Institute, Marseille. References [1] Eisenkop SM, Friedman RL, Wang HJ. Complete cytoreductive surgery is feasible and maximizes survival in patients with advanced epithelial ovarian cancer. Gynecol Oncol 1998;69:103–8. [2] Bristow RE, Tomacruz SR, Armstrong DK, Trimble EL, Montz FJ. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J Clin Oncol 2002;20:1248–59. [3] Coussy F, Che´reau E, Daraı¨ E, et al. Interest of CA 125 level in management of ovarian cancer. Gynecol Obstet Fertil 2011;39(5):296–301. [4] Sugarbaker PH, Jablonski KA. Prognostic features of 51 colorectal and 130 appendiceal cancer patients with peritoneal carcinomatosis treated by cytoreductive surgery and intraperitoneal chemotherapy. Ann Surg 1995;221:124– 32. [5] Harmon RL, Sugarbaker PH. Prognostic indicators in peritoneal carcinomatosis from gastrointestinal cancer. Int Semin Surg Oncol 2005;8:2–3. [6] Tentes AA, Tripsiannis G, Markakidis SK, et al. Peritoneal cancer index: a prognostic indicator of survival in advanced ovarian cancer. Eur J Surg Oncol 2003;29(1):69–73. [7] Che´reau E, Ballester M, Selle F, Cortez A, Daraı¨ E, Rouzier R. Comparison of peritoneal carcinomatosis scoring methods in predicting resectability and prognosis in advanced ovarian cancer. Am J Obstet Gynecol 2010;202(2): 178.e1–178.e10.
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[8] Leblanc E, Querleu D, Narducci F, Occelli B, Papageorgiou T, Sonoda Y. Laparoscopic restaging of early stage invasive adnexal tumors: a 10-year experience. Gynecol Oncol 2004;94:624–9. [9] Manolitsas TP, Fowler JM. Role of laparoscopy in the management of the adnexal mass and staging of gynecologic cancers. Clin Obstet Gynecol 2001;44:495–521. [10] Littell RD, Hallonquist H, Matulonis U, Seiden MV, Berkowitz RS, Duska LR. Negative laparoscopy is highly predictive of negative second-look laparotomy following chemotherapy for ovarian, tubal, and primary peritoneal carcinoma. Gynecol Oncol 2006;103:570–4. [11] Fagotti A, Ferrandina G, Fanfani F, et al. A laparoscopy-based score to predict surgical outcome in patients with advanced ovarian carcinoma: a pilot study. Ann Surg Oncol 2006;13:1156–61. [12] Brun JL, Rouzier R, Uzan S, Daraı¨ E. External validation of a laparoscopic-based score to evaluate resectability of advanced ovarian cancers: clues for a simplified score. Gynecol Oncol 2008;110:354–9. [13] Hudry D, Cannone F, Houvenaeghel G, et al. Comparison of single-port laparoscopy and conventional laparoscopy for extraperitoneal para-aortic lymphadenectomy. Surg Endosc 2013. Epub ahead of print. [14] Fagotti A, Ferrandina G, Fanfani F, et al. Prospective validation of a laparoscopic predictive model for optimal cytoreduction in advanced ovarian carcinoma. Am J Obstet Gynecol 2008;199:642.e1–.e6. [15] Glehen O, Mohamed F, Gilly FN. Peritoneal carcinomatosis from digestive tract cancer: new management by cytoreductive surgery and intraperitoneal chemohyperthermia. Lancet Oncol 2004;5:219–28. [16] Sugarbaker P, Jablonski K. Prognostic features of 51 colorectal and 130 appendiceal cancers with peritoneal carcinomatosis treated by cytoreductive surgery and intraperitoneal chemotherapy. Ann Surg 1995;221:124–32. [17] Sebbag G, Sugarbaker P. Peritoneal mesothelioma proposing for a staging system. EJSO 2001;27:223–4. [18] Sugarbaker P, Chang D, Koslowe P. Prognostic features for peritoneal carcinomatosis in colorectal and appendiceal cancer patients when treated by cytoreductive surgery and intraperitoneal chemotherapy. In: Sugarbaker P.H., editor. Peritoneal carcinomatosis: drugs and diseases. Boston, MA: Kluwer Academic Publishers; 1996. p. 89–104. [19] Sugarbaker P, Chang D. Results of treatment of 385 patients with peritoneal surface spread of appendiceal malignancy. Ann Surg Oncol 1999;6:727–31. [20] Sugarbaker P. Management of peritoneal-surface malignancy: the surgeon’s role. Langenbecks Arch Surg 1999;384(6):576–87. [21] Garofalo A, Valle M. Laparoscopy in the management of peritoneal carcinomatosis. Cancer J 2009;15(3):190–5. [22] Gumbs AA, Milone L, Sinha P, Bessler M. Totally transumbilical laparoscopic cholecystectomy. J Gastrointest Surg 2009;13(3):533–4. [23] Wheeless CR. A rapid, inexpensive, and effective method of surgical sterilization by laparoscopy. J Reprod Med 1969;5:255. [24] Pelosi MA, Pelosi III MA. Laparoscopic supracervical hysterectomy using a single umbilical puncture (minilaparoscopy). J Reprod Med 1992;37: 777–84. [25] Heinemann M, Hamouda S, Petrovic M, et al. Single port surgery and adnexal procedures: which indications in oncological surgery. Gynecol Obstet Fertil 2013;41:421–6. [26] Lambaudie E, Cannone F, Bannier M, Buttarelli M, Houvenaeghel G. Laparoscopic extraperitoneal aortic dissection: does single port surgery offer the same possibilities as conventional laparoscopy. Surg Endosc 2012;26: 1920–3. [27] Morice P, Viala J, Pautier P, Lhomme´ C, Duvillard P, Castaigne D. Port-site metastasis after laparoscopic surgery for gynecologic cancer: a report of six cases. J Reprod Med 2000;45(10):837–40. [28] Mishra A, Keeler B, Maxwell-Armstrong C, Simpson A, Acheson A. The influence of laparoscopy on incisional hernia rates: a retrospective analysis of 1057 colorectal cancer resections. Colorectal Dis 2014. Epub ahead of print. [29] Trastulli S, Cirocchi R, Desiderio J, et al. Systematic review and meta-analysis of randomized clinical trials comparing single-incision versus conventional laparoscopic cholecystectomy. Br J Surg 2013;100(2):191–208. [30] Bresadola F, Pasqualucci A, Donini A, et al. Elective transumbilical compared with standard laparoscopic cholecystectomy. Eur J Surg 1999;165:29–34. [31] Varnoux C, Huchon C, Bats AS, et al. Diagnostic accuracy of hand-assisted laparoscopy in predicting resectability of peritoneal carcinomatosis from gynecological malignancies. Eur J Surg Oncol 2013;39(7):774–9.
Contents lists available at ScienceDirect
European Journal of Obstetrics & Gynecology and Reproductive Biology journal homepage: www.elsevier.com/locate/ejogrb
Evaluation of single-port laparoscopy for peritoneal carcinomatosis assessment in advanced ovarian cancer Delphine Quaranta *, Eric Lambaudie, Mellie Heinnemann, Gilles Houvenaeghel, Elisabeth Che´reau Department of General and Oncological Surgery, Paoli Calmettes Institute, 232 Boulevard Sainte-Marguerite, 13273 Marseille, France
A R T I C L E I N F O
A B S T R A C T
Article history: Received 29 January 2014 Received in revised form 4 July 2014 Accepted 20 July 2014
Objectives: Ovarian cancers are usually diagnosed at an advanced stage. The extent of the disease before surgery partly determines the ability to perform a complete cytoreduction. The peritoneal cancer index (PCI) is used to evaluate peritoneal carcinomatosis and has been validated in ovarian cancer and correlated with resectability. The aim of our study was to assess the feasibility of single-port laparoscopy (SPL) for suspicion of advanced ovarian cancer and to describe the ability to calculate the PCI score at the time of laparoscopy. Study design: Between February 2011 and January 2013, 33 patients underwent SPL for suspected advanced ovarian cancer. Individual records for all patients were prospectively reviewed and analyzed. For each patient, we determined the PCI score. Results: 33 patients underwent initial SPL, 85% had increased carcinological markers and 67% a radiological suspicion of peritoneal carcinomatosis. The median operative time was 90 min. During SPL, 76% of patients underwent ascites evacuation; all patients had peritoneal cytology and peritoneal biopsies. Only 3 patients experienced perioperative complications. Two open conversions were recorded. Quotation of the PCI score was possible for all patients. Eighteen patients (55%) had a PCI score below 10; one had a maximal PCI score of 39. The PCI score was null for 9 patients. Non-browsing areas marked 8 procedures. Conclusions: SPL appeared to be feasible, with satisfying immediate results and postoperative outcome, compared to conventional laparoscopy. It allowed a satisfying exploration of the abdomino-pelvic cavity and a good description of peritoneal carcinomatosis with only a few non-browsing PCI areas. ß 2014 Elsevier Ireland Ltd. All rights reserved.
Keywords: Single-port laparoscopy Peritoneal carcinomatosis PCI score Advanced ovarian cancer
Introduction Ovarian cancers are usually diagnosed at an advanced stage, with massive, widespread intra-abdominal disease. Multiple studies reported that the completeness of the primary cytoreductive surgery independently influences survival for these patients [1,2]. Median and five-year survivals after removal of all visible disease (complete cytoreduction) were reported to exceed survival rates resulting from suboptimal procedures (residual disease 1 cm)[2]. The extent of the disease before surgery partly determines the ability to perform a complete
* Corresponding author at: Universitary hospital Archet2, Department of Gynecology and Obstetrics, 151 Route de saint-antoine de ginestiere, 06200 Nice, France. Tel.: +00 33 4 91 22 35 32; fax: +00 33 4 91 22 36 13. E-mail address: [email protected] (D. Quaranta). http://dx.doi.org/10.1016/j.ejogrb.2014.07.008 0301-2115/ß 2014 Elsevier Ireland Ltd. All rights reserved.
cytoreduction. The ability to predict complete resection at the time of diagnosis could be suggested during the preoperative course with a clinical examination, a CA125 level check or radiological examinations. However, it has been demonstrated that these data were insufficient to predict with precision resectability [3]. To quantify with more precision the intra-abdominal extent of the disease, a number of numerical ranking systems have been proposed and could be used during the first step of surgery. The most described was the peritoneal cancer index (PCI), used to evaluate the peritoneal spread in malignant intraperitoneal and pelvic tumors [4,5]. Its use for ovarian cancer has also been reported and its correlation with resectability has been demonstrated in advanced ovarian cancer [6,7]. The performance of a laparoscopy to determine resectability has been demonstrated for advanced ovarian cancer and specific scores were proposed [8–12]. However, some studies underlined the possibility of post site metastasis. In this setting, the use of a
D. Quaranta et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 181 (2014) 60–65
single port could allow a better exploration and description of peritoneal carcinomatosis (2 to 3 instruments in addition to a camera), no additional scar and a larger biopsy for diagnosis. To date, to our knowledge, no study has reported the exploration of peritoneal carcinomatosis using a single-port approach. The aim of this study was to assess the feasibility of a singleport exploratory laparoscopy for suspected advanced ovarian cancer and to describe the ability to calculate the PCI score at the time of the laparoscopy. Materials and methods Patient population Between February 2011 and January 2013, 33 consecutive patients underwent a laparoscopy for suspected advanced ovarian cancer in Paoli-Calmettes Institute, Marseille, France. Individual records for all patients were prospectively analyzed: patient and tumor characteristics, per-operative findings and postoperative course. For each patient, we determined the PCI score. Peritoneal cancer index (PCI) Sugarbaker first described the PCI for colon cancer in 1995 [4]. A few years later, Tentes et al. evaluated the PCI for ovarian cancer [6]. The PCI quantitatively combines the distribution of the tumor throughout 13 abdomino-pelvic regions with a lesion size (LS) score. Lines define nine regions, which are numbered in a clockwise direction, with zero at the umbilicus and one defining the space beneath the right hemidiaphragm. Regions 9 to 12 divide the small bowel into upper and lower jejunum and upper and lower ileum. Each region is also defined by the anatomic structures found there. The LS score is determined after complete lysis of all adhesions. LS-0 means no visible tumor; LS-1 indicates implants less than 0.5 cm in size, LS-2 between 0.5 and 5 cm, and LS-3 greater than 5 cm. This refers to the largest diameter of tumor implants. If there is a confluence of disease matting abdominal or pelvic structures together, this is automatically scored as LS-3. The LS are then summed for all abdomino-pelvic regions. A numerical score from 0 to 39 indicates the extent of the disease within all regions. In the report by Tentes et al. [6], there was a significant difference in the five-year survival rates between patients with a PCI > 10 and 10. A previous study demonstrated the ability of the PCI to predict resectability, post-operative morbidity and outcome in advanced ovarian cancer [7].
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average BMI was 24 Kg/m2 (range: 17–42). Seventy-five percent of the patients had a history of abdominal surgery and six patients had previous cancer history (Table 1). In 76% of cases (n = 25), SPL was performed for clinical or radiological ascites. For 28 of the 33 patients (85%), SPL was motivated by an increase of carcinological markers, and for 22 of patients (67%), by radiological suspicion of peritoneal carcinomatosis (Table 2). The median operative time, from initial umbilical section to last skin stitch, was 90 min (range: 30–188 min). Surgical characteristics are reported in Table 3. During SPL, 25 patients (76%) underwent ascites evacuation. Peritoneal cytology and peritoneal biopsies were performed for all patients. In a few cases, surgical resections were made (4 oophorectomies and 1 salpingectomy). One patient had a bacteriological study of a thickened and purulent peritoneal fluid. Three patients experienced perioperative complications: two small-bowel injuries and one bladder injury. Two open conversions were recorded because of exploration difficulties (adhesions or small bowel injuries). No perioperative transfusion and no major complication occurred. The median hospital stay was 1.84 days (range: 0–12 days). Quotation of the PCI score was possible for all patients (Table 4). Eighteen patients (55%) had a PCI score below 10, one patient had a maximal PCI score of 39 (Fig. 2). The PCI score was null for nine patients. Non-browsing areas marked eight procedures (24%). Three patients had two or more than two non-browsing areas: one for malignant lymphoma and two patients because of major extensive carcinomatosis (Table 5). Region 6, corresponding to the pelvic area, could not be explored in six patients because of blinded pelvis and adhesions. This observation’s failure was noticed in 2 cases for the region ‘‘left lower’’ (region 5) and also for each of the following regions ‘‘right upper’’ (region 1), ‘‘left upper’’ (region 3), ‘‘right lower’’ (region 7), ‘‘upper jejunum’’ (region 9) and ‘‘lower jejunum’’ (region 10) [4]. Comments
The patient was placed in the dorsal decubitus position, and one 3-cm incision was performed across the umbilicus and the single port was installed. As reported previously for extraperitoneal para-aortic lymphadenectomy, we used a single port GelPOINT1 device (Applied Medical) (Fig. 1) [13]. The peritoneal cavity was inflated with carbon dioxide up to a maximum pressure of 10 mmHg. We used a 10 mm laparoscope and 5 mm standard instruments, including fenestrated forceps, bipolar forceps, and monopolar scissors if necessary. No additional trocar was used.
A single-port laparoscopic approach has been recently developed and evaluated. As already reported, it appeared to be feasible, with a satisfying immediate result and post-operative outcome, compared to conventional laparoscopy [13]. It also allowed a reliable evaluation of peritoneal carcinomatosis of our 33 patients, even though 76% of them had undergone previous abdominal surgery. In our study, for 76% of the patients the PCI score has been calculated without missing an area. A median operative time of 90 min, limited hospital stay and absence of major complications also highlighted its interest. Indeed, before surgery, the ability to perform a complete primary cytoreduction is influenced by the extent of disease. Multiple studies have reported that residual disease after surgery was the best predictive factor for survival [2]. In the aim to select patients eligible for complete surgery, surgeons need the tools to establish the precise extent of the disease. In this setting, the FIGO classification is insufficient. Consequently, more detailed quotation systems are necessary at the time of surgery. One previous study has compared the ability of various carcinomatosis scores to predict the extent of the disease in relation to resectability. In this study, PCI and Fagotti modified scores were the most pertinent [1,7]. They outperformed Fagotti and Eisenkop scores [11,14].
Results
PCI score
Thirty-three patients underwent an initial single-port laparoscopy (SPL) in the context of suspected advanced ovarian cancer. The median age of the patients was 62 years (range: 32–84). The
The PCI score gives valuable information about the precise distribution of seeding and tumor volume, representing in detail the peritoneal extent [15]. For ovarian cancer, Tentes et al. reported
Surgical management
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Fig. 1. GelPOINT1, device and installation steps.
that the mean survival and five-year survival rate for patients with a PCI 10 were 80 12 months and 65%, respectively, while the mean survival and five-year survival rate for patients with a PCI > 10 were 38 7 months and 29%, respectively [5]. The PCI score was correlated with survival (p = 0.0253) in their study. Other studies found that a score superior to 10 compromised the ability of optimal surgical management without carcinomatous residue [4,16–19].
Nevertheless, there are some limitations for the use of the PCI score. First, the PCI score might be misevaluated by the existence of non-invasive malignant tumors, such as peritoneal pseudomyxoma, grade 1 sarcoma, and some peritoneal mesothelioma, which could be completely resected. So, a high PCI score might be reduced to a null score after cytoreduction, which means that prognosis does not have to be based on the PCI score only. Secondly, the
D. Quaranta et al. / European Journal of Obstetrics & Gynecology and Reproductive Biology 181 (2014) 60–65 Table 1 Patients characteristics. Patients characteristics
n (%), [range]
Age (years) BMI (kg/m2) Previous surgical history -Laparoscopy -Laparotomy -Caesarean Previous neoplasic diseases -Breast -Kidney -Cardia -Endometrial -Ovary
62 [32–84] 24 [17.4–42.55]
the large amount of patients with a previous history of surgery, this result could be considered satisfactory. This rate is below the rate described by Garofalo, but in our study, patients with nonresectable disease underwent neo-adjuvant chemotherapy [21]. The aim of the laparoscopy was to perform a diagnosis biopsy and to conduct exploration to determine resectability with minimal adhesiolysis and morbidity.
18 (54%) 5/33 (15%) 4/33 (12%) 6/33 (18%) 2/33 (6%) 1/33 (3%) 1/33 (3%) 1/33 (3%) 1/33 (3%)
Single-port laparoscopy
Table 2 Indications of laparoscopy. Laparoscopy indication
n
%
Ascites clinic/radiologic Ovarian/pelvic mass on radiological exams Increase of carcinologic markers CA 15.3 CA 125 SCC ACE Ca 19.9 Radiological suspicion of peritoneal carcinomatosis
25 24 6 24 2 2 1 22
76 72 18 73 6 6 3 67
Table 3 Surgical characteristics. Surgical characteristics
n
Operative time (min) Per operative actions Ascites evacuation
0 <500 cm3 500 cm3
Adhesiolysis Peritoneal cytology Peritoneal bacteriology Peritoneal biopsies -Without visible lesions -Supra-millimeter lesions -Infra-millimeter lesions Epiploon systematically suspicious epiploon Sigmoid lesion Rectal lesion Gastric lesion Biopsy of ovarian tumor Surgical resection -Annexectomy -Salpingectomy Per operative complications Per operative transfusions injuries -Small bowel injury -Bladder injury Open conversion to laparotomy Length of hospitalization (days, range)
3 7 25 3 8
5 4 1 0 3 2 1 2 1.84
63
Range (%) 90
30–188
8 11 14 6 33 1
24% 33% 42% 18% 100% 3%
9% 21% 76% 9% 24% 2 3 1 1 15% 12% 3% 5 0% 9% 6% 3% 6% 1–12
6% 9% 3% 3%
15%
Table 4 Peritoneal carcinomatosis index (PCI). PCI score
10
11–20
21–30
31–39
Number of patients (%)
18 (54%)
4 (12%)
10 (30%)
1 (3%)
invasion of some anatomic regions, such as hepatic pedicle with the common bile duct, are inoperable and compromises the prognosis, even though the PCI score is low [20]. In our study, only in 24% of patients did we fail to calculate the exact PCI score because of non-browsing areas. Taking into account
The fundamental interest of SPL lies in having one single incision for all laparoscopic instruments. However, the major drawback with SPL is the absence of ‘‘triangulation’’ which could be technically difficult for laparoscopic surgeons. Each pharmaceutical industry has adopted its own nomenclature for this procedure. The procedure is usually named laparo-endoscopic single-site surgery (LESS) [22]. The Triport (Advanced Surgical Concepts, Wicklow, Ireland), also called R-Port, is a device designed to be used through a unique incision, typically across the umbilicus, because of the fascial defect. This device has been approved by the Food and Drug Administration (FDA). In gynaecology, the first example of SPL was tubal ligation by Wheeless [23]. A single-port laparoscopic hysterectomy with bilateral salpingo-oophrectomy has been reported by Pelosi [24]. GelPOINT1 SPL has been recently described in the Paoli-Calmettes Institute in different surgical indications, such as adnexal procedures or extraperitoneal para-aortic lymphadenectomy [13,25,26]. To our knowledge, no study has reported the use of SPL for the evaluation of resectability in advanced ovarian cancer. To install the GelPOINT SPL an aneurotic incision of 2–3 cm is needed. The peritoneal surface of the shaft contains an autoexpendable ring, which allows a sealing, whatever the thickness of the abdominal wall. The external part of the GelPOINT1 contains three triangular ports incorporated in a gelatinous material, and an opening dedicated to insufflation and maintenance of pneumoperitoneum. The concept of ‘‘triangulation’’ is the main principle of singleport surgery. It allows a good overview and an ergonomic position for the surgeon and his assistants. Hence, the umbilicus appeared to be the most appropriate site for the device. The Triport presents many advantages. First, there is a cosmetic advantage: several instruments of variable sizes could be introduced by one unique incision, through the GelPOINT’s three trocars, without losing pneumoperitoneum. Secondly, there is a carcinologic advantage: in the case of disseminated peritoneal carcinomatosis, the unique incision allows a histological diagnosis and limits the classical carcinomatous dissemination through the site ports [27]. Indeed, port-site dissemination has been described in observations of conventional laparoscopy and removal of the port sites during debulking surgery in advanced ovarian cancer is recommended. Moreover, Alexis spacer, included in the GelPOINT device, is used as a abdominal wall protector. The third advantage is technical: the GelPOINT1 device is easily introduced and removed. The thickness of the abdominal wall is not an obstacle for single-port use. The last advantage highlights the lower morbidity of SPL, compared to conventional laparoscopy: it decreases perioperative complications (vascular, digestive and adjacent organ injuries), post-operative complications (less incidences of hernia, and better cosmetic results) and length of hospital stay [13,28]. The single port might also limit post-operative pain, as suggested in a systematic review [29]. However, the preference for umbilical positioning might be an obstacle when targeted tissue is located too far from the instruments’ articulation. Moreover, it could be difficult to introduce GelPOINT1 SPL elsewhere other than through an abdominal defect.
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Fig. 2. Pictures of peritoneal carcinomatosis.
Table 5 Non-browsing areas. Patients Patient Patient Patient Patient Patient Patient Patient Patient
2 5 12 14 17 21 23 30
Non-browsing areas
Characteristics
Areas 5 and 6 Area 1 Area 3 Areas 5, 6 and 7 Area 6 Areas 6, 9 and 10 Area 6 Area 6
Blinded pelvis-lymphoma Post-operative adhesions Non visible left hemi-diaphragm-carcinomatosis Blinded pelvis-carcinomatosis/adhesions Blinded pelvis-carcinomatosis/adhesions Extensive carcinomatosis Adhesions Adhesions
Because of the ‘‘triangulation’’, manipulation of the camera might cause the involuntary movement of the adjacent instruments. This could increase the difficulties in achieving easy tasks [30]. Using a single-port trocar enforces a restricted external area for the surgeon’s hands, compared to a standard laparoscopy. Indeed, the instruments and the laparoscope are in competition through a unique opening, both on the outside (conflict between hands) and on the inside (conflict of the instruments’ extremity). So, it is essential to develop and distribute empowered instruments that
provide: good articulation, variable sizes, and remote-articulated handles from the entrance trocar, as well as low-profile cameras with Wi-Fi optics. The insufflation tube has to be positioned so as not to interfere with the other instruments. All these measures would free external space and limit collisions. In conventional laparoscopy, a switch of instruments or camera in different ports avoids bad exposure. In SPL, this adaptation is impossible, threatening operative exposure and consequently safety. Using flexible instruments and angular optics could improve exposure and reduce the problem of non-browsing areas.
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Exploration of region 3 ‘‘left upper’’, which contains the splenic area, could be more precise with the use of a 308 angular optics, for example. Recently a new technique for assessing the extent of peritoneal carcinomatosis was described, combining manual palpation and standard laparoscopy. Hand-assisted laparoscopy may perform better than laparoscopy alone for predicting the resectability of peritoneal carcinomatosis by increasing the number of sites evaluated [31]. SPL with a unique incision is a new, attractive technology, of interest to investors, surgeons and patients. As reported in our study, this procedure allows the diagnosis of neoplasic disease by enabling samplings such as peritoneal cytology, biopsy. More particularly, its feasibility relies in the calcul of PCI score, allowing a satisfying exploration of the abdomino-pelvic cavity. The precision of SPL is influenced by the surgeon’s experience and a precise knowledge of the PCI score. Ideally, a unique experienced operator should manage the initial laparoscopy with the PCI evaluation and debulking surgery. Conflict of interest statement All authors declare no conflict of interest. Condensation The peritoneal cancer index is validated for laparotomic evaluation of peritoneal carcinomatosis in ovarian cancer. We have assessed the advantages and feasibility of single-port laparoscopy. Acknowledgement The authors thank the staff of Paoli Calmettes Institute, Marseille. References [1] Eisenkop SM, Friedman RL, Wang HJ. Complete cytoreductive surgery is feasible and maximizes survival in patients with advanced epithelial ovarian cancer. Gynecol Oncol 1998;69:103–8. [2] Bristow RE, Tomacruz SR, Armstrong DK, Trimble EL, Montz FJ. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J Clin Oncol 2002;20:1248–59. [3] Coussy F, Che´reau E, Daraı¨ E, et al. Interest of CA 125 level in management of ovarian cancer. Gynecol Obstet Fertil 2011;39(5):296–301. [4] Sugarbaker PH, Jablonski KA. Prognostic features of 51 colorectal and 130 appendiceal cancer patients with peritoneal carcinomatosis treated by cytoreductive surgery and intraperitoneal chemotherapy. Ann Surg 1995;221:124– 32. [5] Harmon RL, Sugarbaker PH. Prognostic indicators in peritoneal carcinomatosis from gastrointestinal cancer. Int Semin Surg Oncol 2005;8:2–3. [6] Tentes AA, Tripsiannis G, Markakidis SK, et al. Peritoneal cancer index: a prognostic indicator of survival in advanced ovarian cancer. Eur J Surg Oncol 2003;29(1):69–73. [7] Che´reau E, Ballester M, Selle F, Cortez A, Daraı¨ E, Rouzier R. Comparison of peritoneal carcinomatosis scoring methods in predicting resectability and prognosis in advanced ovarian cancer. Am J Obstet Gynecol 2010;202(2): 178.e1–178.e10.
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