Surgery, Gastroenterology and Oncology

Ovarian cancer is the most common cause of lethality among women with gynecological cancers. In Europe, it ranks fifth in frequency in women after malignancies of the mammary gland, colon, lung and uterine body. Generally, it is diagnosed at an advanced stage (III-IV) due to the non-specificity of symptoms in the early stage and the lack of effective screening methods. The majority of patients with advanced epithelial ovarian cancer are indicated either for neoadjuvant chemotherapy followed by optimal cytoreduction or optimal cyto-reduction followed by adjuvant chemotherapy. This necessitates laparotomy or laparoscopy for the purpose of histological verification of the tumor and assessment of optimal cyto-reduction. A laparoscopically based system has been created, anticipating the possibility of optimal cytoreduction. In the present article, we describe the Fagotti’s laparoscopic score in advanced epithelial ovarian cancer and briefly discuss its strengths and limitations.

INTRODUCTION

Ovarian cancer is the most common cause of death among women with gynecological cancers (1). In Europe, it ranks fifth in frequency in women (1) after malignancies of the mammary gland, colon, lung and uterus. Generally, it is diagnosed in an advanced stage of the disease with peritoneal or lymph node metastases in the upper abdomen due to the non-specificity of symptoms in the early stage and the lack of effective screening methods (1). The majority of patients with advanced epithelial ovarian carcinoma (AEOC) are indicated either for neoadjuvant chemotherapy followed by optimal cytoreduction (RO) or optimal cytoreduction followed by adjuvant chemotherapy. The latter is the cornerstone in the management of AEOC as it is associated with increase survival (1-3). Unfortunately, clinical examination, laboratory tests and different imaging modalities are not always sufficient to differentiate the two cohorts of patients – the ones that are firstly indicated for neoadjuvant chemotherapy followed by optimal cytoreduction and the others that are candidates for optimal cytoreduction followed by adjuvant chemotherapy. This necessitates laparotomy or laparoscopy in order to predict the possibility of optimal cytoreduction and histological verification of the tumor. A laparoscopically based system has been created, anticipating the possibility of optimal cyto-reduction (2,4). In the present article, we describe the Fagotti’s laparoscopic score in AEOC and briefly discuss its strengths and limitations. Additionally, we provide laparoscopic figures of the anatomical zone of the abdomen affected by disseminated ovarian cancer.

Explorative Laparotomy vs Exploratory Laparoscopy

The inferiority of exploratory laparotomy compared to exploratory laparoscopy in patients with AEOC is the following (2):

1. Longer recovery and longer hospital stay;

2. High incidence of complications of the anterior abdominal wall – hematomas, abscesses, hernias, eventrations (common - due to low levels of serum albumin in these patients);

3. Poorer postoperative pain control;

4. Slower postoperative recovery and poorer quality of life;

5. Delay of neoadjuvant treatment.

Minimally invasive surgery offers the advantage of shorter hospital stay, decreased perioperative recovery, less postoperative pain, lower rates of wound infections and hernias. (3) The hospital stay after laparoscopic evaluation is shorter compared to laparotomic one. Therefore, patients, who underwent exploratory laparoscopy are initiated for adjuvant/neoadjuvant treatment faster compared to the laparotomy cohort arm.

Fagotti’s Laparoscopic Score

In 2006, Anna Fagotti et al. introduced a laparoscopic scoring system evaluating the possibility of optimal cytoreduction in AEOC. The system has been well accepted and has rapidly gained popularity in the gynecologic oncology community. The aim of the Fagotti’s laparoscopic score was to create a more objective quantitative laparoscopic model for predicting the chances of optimal cytoreductive surgery in AEOC (4).

The Fagotti’s scoring system is based on the presence or absence of metastases in 7 anatomical regions:

1. Greater omentum;

2. Parietal peritoneum (the exception is the diaphragmatic parietal peritoneum);

3. Parietal peritoneum of the diaphragmatic parietal peritoneum;

4. Mesentery;

5. Stomach;

6. Small and large intestines;

7. Liver.

The anatomical regions evaluated by the Fagotti’s score are shown in fig. 1.

Figure 1 - Anatomical areas in the Fagotti’s score examining the presence of metastases (authors' own material):

1. Omentum;
2. Parietal peritoneum;
3. Diaphragmatic parietal peritoneum;

4. Mesentery;
5. Stomach;
6. Small and large intestines;
7. Liver

In the presence of massive metastases, the anatomical area is evaluated with 2 points, and in the absence or isolated metastases – with 0 points. The maximal score of points is 14 and the minimum is 0. The pelvis is excluded from the system, as in AEOC, the pelvic tumors are always resectable (by Hudson’s operation or/without rectal/sigmoid resection). The authors concluded that a score equal to or greater than 8 points is associated with suboptimal cytoreduction and the presence of residual tumor. It is necessary to emphasize that during the creation of the Fagotti’s, system for optimal cytoreduction was considered R<1 cm (4). The scoring system of the Fagotti’s laparoscopic score in AEOC is shown in table 1.

Table 1 - Fagotti’s scoring system in advanced epithelial ovarian cancer

Greater omentum

Evaluation of the greater omentum includes the tumor infiltration of the greater omentum up to the large curvature of the stomach (infiltration of supracolic omentum). Score 2 – “omental cake” with metastases reaching the grater curvature of the stomach (fig. 2). Score 0 – no metastases or isolated single metastases (5).

Figure 2 - Omentum - "omental cake" – score 2 (authors' own material).

a, b – “omental cake” in patients with advanced epithelial ovarian cancer.

Parietal peritoneum

Score 2 – massive miliary parietal carcinomatosis or unresectable massive and multiple metastases in the parietal peritoneum (fig. 3).

Score 0 – an absence of metastases or cases of peritoneal carcinomatosis covering isolated anatomical areas – the paracolic gutters (5).

Figure 3 - Massive carcinomatosis of the parietal peritoneum in patients with advanced epithelial ovarian cancer – score 2. (a, b - authors' own material)

Diaphragmatic parietal peritoneum

Score 2 – massive miliary parietal carcinomatosis or unresectable massive confluent metastases on the diaphragmatic parietal peritoneum (fig. 4, 5).

Score 0 – an absence of metastases (5).

Figure 4 - Massive military parietal carcinomatosis on the right (a) and left (b) diaphragmatic parietal peritoneum (authors’ own material). Score 2 in both figures.

Figure 5 - Unresectable massive confluent metastases

on the right diaphragmatic parietal peritoneum – score 2 (authors' own material).

Mesentery

Score 2 – a presence of confluent carcinomatosis along the mesentery or the presence of a tumor in the area of the mesenteric root (fig. 6).

Score 0 - absence of metastases or the presence of single insignificant metastases that can be treated with bipolar coagulation (5).

Evaluation of the mesentery is performed by laparoscopic small bowel traction to the anterior abdominal wall or cranially. In the presence of rigidity and mesentery retraction the score is 2.

Figure 6 - Multiple mesenteric metastases (figure A,B) – score 2 (authors' own material)

Stomach

Score 2 – a presence of macroscopically visible metastasis infiltrating the stomach wall (fig. 7).

Score 0 – absence of metastases or presence of single superficial metastases involving only the visceral peritoneum (5).

Small and large intestines

Score 2 – a presence of multiple confluent metastases or the presence of massive miliary carcinomatosis (fig. 8).

Score 0 – no metastases or single visceral peritoneum metastases that do not require bowel resection and can be removed by bipolar coagulation. (5)

Liver

Score 2 – in the presence of superficial (involving Glisson's capsule) liver metastases.

Score 0 – absence of metastases on the surface of the liver.

Laparoscopic Aspects of Fagotti’s Score

When Fagotti scoring system scoring is performed, we always use open laparoscopic access (Hasson's technique) (1) below or above the level of the umbilicus for the following reasons:

1. Patients with advanced ovarian carcinoma have ascites - aspiration of the ascites fluid before insufflation is desirable (2).

1. The frequent presence of adhesions of the omentum and the intestine within the anterior abdominal wall due to the advanced stage of the disease.

Access through the navel is not desirable due to the possible implantation of metastases at the trocar site, the so-called “port site metastases” (2).

When cutting the peritoneum, we always feel with circular movements with a finger the place of insertion of the first trocar in the abdominal cavity.

The Fagotti’s scoring system is used to differentiate the following patients (2):

1. Patients candidates for optimal cytoreduction and adjuvant chemotherapy.

2. Patients candidates for neoadjuvant chemo-therapy and eventual subsequent cytoreduction.

3. Patients, who have already underwent neo-adjuvant chemotherapy and subsequent evaluation for the possibility of secondary optimal cytoreduction.

Update of the Fagotti’s Scoring System

In 2015, an article was published with an update of the Fagotti’s scoring system, which highlighted that the involvement of the mesenteric root by the tumor has always been a contraindication for surgical treatment of AEOC, and its presence in the Fagotti’s scoring system is not feasible. Additionally, the presence of multiple miliary metastases in the visceral peritoneum of the small intestine and mesentery also leads to suboptimal cytoreduction and the presence of macroscopic residual tumor (6).

These zones were excluded from the new Fagotti’s scoring system as they lead to suboptimal debulking. One of the main reasons is that, currently no residual macroscopic tumor is considered for optimal cyto-reduction (6). Additionally, the tumor involvement of the lesser omentum and the spleen was incorporated to the stomach anatomical area of the updated Fagotti’s laparoscopic scoring system (6,7). Rectal and sigmoid metastases leading to recto-sigmoid resection were excluded from the score because they are located in a pelvis and are part of the standard Hudson’s procedure, when resection of the rectum/sigma is indicated (7). The size of the superficial liver metastases should be more than 2 cm in the update of the score (5). Update of the score is summarized in
table 2.

Table 2 - Update of the Fagotti's scoring system in advanced epithelial ovarian cancer

The recent improvement of the upper abdominal surgery among oncogynecologists has increased the score, which is associated with optimal debulking surgery (R0) – equal to or less than 10 (6,7). Fagotti’s often mentions that the main purpose of the scoring system is rather to avoid unnecessary laparotomies (in Fagotti’s score more than 10). Regarding the possibility of optimal cytoreduction - the sensitivity of the method is comparatively lower (4,7).

DISCUSSION

In this review article, we want to emphasize the strengths and limitations of the Fagotti’s laparoscopic scoring system. The main standard of care in AEOC patients is primary cytoreductive surgery followed by adjuvant chemotherapy. The Fagotti’s laparoscopic scoring system was widely accepted among oncogynecologists.

Most authors concluded that there is no accurate scoring system to predict the possibility of optimal cytoreduction (8,9). Laparoscopic evaluation of AEOC is not included in most treatment guidelines for the disease (9). The authors mention that laparoscopy is useful tool in order to avoid unnecessary laparotomy in cases of advanced disease when it is impossible to achieve optimal cytoreduction and it is a useful in the decision making on treatment selection (8,9).

Although the Fagotti’s scoring system is the most widely used laparoscopic score, there are other scoring systems that predict the chance of achieving optimal cytoreduction in AEOC (10-13). However, some of these scoring system are based either on laparotomic evaluation or imaging modalities and laboratory test.

The Eisenkop score intraoperatively evaluates 5 anatomic regions – the right and left upper quadrants, pelvis, retroperitoneum and central abdomen. Each region is valued between 0 and 3 points (10).

Jacquet and Sugarbaker were the first to propose the Peritoneal Cancer index (PCI) (11). It is assessed by inspection of the peritoneum during laparotomy, and it includes 9 abdominal regions. A higher PCI is associated with suboptimal cytoreduction and high risk of complications and reduced survival rate (11).

The Suidan score system is a non-invasive model based on eight radiological criteria through CT assessment and three clinical criteria (age ≥ 60 years, CA-125 ≥ 500 U/mL, ASA 3–4) (12). These radiological findings consist of lesions in the splenic hilum, gastrohepatic

ligament/porta hepatis, retroperitoneal lymph nodes above the renal hilum, diffuse small bowel adhesions or thickening, abdominal ascites, gallbladder fossa/liver intersegmental fissure lesion, lesser sac lesion more than 1 cm and root of the superior mesenteric artery lesion (12).

There are others scoring system, which estimates the surgical complexity during AEOC debulking surgery (14).

Diagnostic imaging can provide a preoperative systematic report of tumor dissemination and has a high diagnostic performance for prediction of bulky disease, but it is less accurate for small-volume carcinomatosis, which may lead to unnecessary laparotomies. Laparoscopy has its place in combination with imaging in cases where imaging results regarding respectability are unclear (7). Laparoscopy can be used as a second-stage diagnostic tool to exclude carcinomatosis on bowel and its mesentery. Nevertheless, The Fagotti’s scoring system has some limitations. (2) In case of multiple adhesions due to previous surgeries or previous inflammatory diseases, the laparoscopic evaluation of some of the anatomical areas could not be feasible (1). Some anatomical areas are difficult to access by laparoscopy (7) - the omental bursa, the splenic hilum, porta hepatis, gastrosplenic ligament. The retroperitoneal lymph nodes (pelvic, paraaortic, celiac) are not included in the Fagotti’s scoring system, because of the failure of laparoscopy to carefully access these spaces. Deep vascular infiltration by metastatic lymph nodes can be a reason of unresectability, nevertheless the lymph-nodal evaluation was excluded from the score (4).

Despite the low accuracy of imaging modalities in the prediction of residual disease, the preoperative imaging maintains an important diagnostic role in the evaluation of tumor spread in anatomical sites not explorable with laparoscopy (such as the retroperitoneum, the retro-hepatic area and the porta hepatis), and in the diagnosis of parenchymal and lymphatic metastasis (13,15). Indeed, a multimodal approach is crucial for the pre-operative evaluation of patients with AEOC and laparoscopy is the best tool to evaluate the diaphragmatic, peritoneal and omental spread of the disease (3,13,16).

The worldwide application of the Fagotti's laparoscopic score in AOEC patients according to different studies is summarized in table 3.

Table 3 - Application of the Fagotti’s laparoscopic score in advanced epithelial ovarian cancer according to different studies

CONCLUSION

The Fagotti’s laparoscopic scoring system in women with AEOC leads to a reduction in cases of redundant laparotomy in inoperable patients. Moreover, it is safe and easily available surgical procedure, which decrease the hospital duration, improve the quality of life and reduce complications in inoperable patients. The laparoscopic score system should be always combined with preoperative clinical, paraclinical and imaging modalities.

Author’s Contribution

All authors have accepted responsibility for the entire content of this manuscript and approved its submission.

Competing Interests

Authors state no conflict of interest.

Research Funding: None declared.

Research Ethics: Not applicable due to the review nature of the article.

Informed Consent: Not applicable.

Data Availability

The authors declare that all related data are

available concerning researchers by the corresponding author’s email.

REFERENCES

1. Tomar TS, Nair RP, Sambasivan S, Krishna KMJ, Mathew A, Ahmed IM. Role of laparoscopy in predicting surgical outcomes in patients undergoing interval cytoreduction surgery for advanced ovarian carcinoma: A prospective validation study. Indian J Cancer. 2017; 54(3):550-555.

2. Fagotti A, Perelli F, Pedone L, Scambia G. Current Recommendations for Minimally Invasive Surgical Staging in Ovarian Cancer. Curr Treat Options Oncol. 2016;17(1):3.

3. Feng Z, Wen H, Jiang Z, Liu S, Ju X, Chen X et al. A triage strategy in advanced ovarian cancer management based on multiple predictive models for R0 resection: a prospective cohort study. J Gynecol Oncol. 2018;29(5):e65.

4. Fagotti A, Ferrandina G, Fanfani F, Ercoli A, Lorusso D, Rossi M et al. A laparoscopy-based score to predict surgical outcome in patients with advanced ovarian carcinoma: a pilot study. Ann Surg Oncol. 2006;13(8):1156-61.

5. Fagotti A, Ferrandina G, Fanfani F, Garganese G, Vizzielli G, Carone V et al. Prospective validation of a laparoscopic predictive model for optimal cytoreduction in advanced ovarian carcinoma. Am J Obstet Gynecol. 2008;199(6):642.e1-6.

6. Petrillo M, Vizzielli G, Fanfani F, Gallotta V, Cosentino F, Chiantera V et al. Definition of a dynamic laparoscopic model for the prediction of incomplete cytoreduction in advanced epithelial ovarian cancer: proof of a concept. Gynecol Oncol. 2015;139(1):5-9.

7. Pinto P, Burgetova A, Cibula D, Haldorsen IS, Indrielle-Kelly T, Fischerova D. Prediction of Surgical Outcome in Advanced Ovarian Cancer by Imaging and Laparoscopy: A Narrative Review. Cancers (Basel). 2023;15(6):1904.

8. Rutten MJ, Leeflang MM, Kenter GG, Mol BW, Buist M. Laparoscopy for diagnosing resectability of disease in patients with advanced ovarian cancer. Cochrane Database Syst Rev. 2014;2014(2): CD009786.

9. Fotopoulou C, Hall M, Cruickshank D, Gabra H, Ganesan R, Hughes C et al. British Gynaecological Cancer Society (BGCS) epithelial ovarian / fallopian tube/primary peritoneal cancer guidelines: recommendations for practice. Eur J Obstet Gynecol Reprod Biol. 2017;213:123-139.

10. Eisenkop SM, Spirtos NM, Friedman RL, Lin WC, Pisani AL, Perticucci S. Relative influences of tumor volume before surgery and the cytoreductive outcome on survival for patients with advanced ovarian cancer: a prospective study. Gynecol Oncol. 2003;90(2): 390-6.

11. Jacquet P, Sugarbaker PH. Clinical research methodologies in diagnosis and staging of patients with peritoneal carcinomatosis. Cancer Treat Res. 1996;82:359-74.

12. Suidan RS, Ramirez PT, Sarasohn DM, Teitcher JB, Mironov S, Iyer RB et al. A multicenter prospective trial evaluating the ability of preoperative computed tomography scan and serum CA-125 to predict suboptimal cytoreduction at primary debulking surgery for advanced ovarian, fallopian tube, and peritoneal cancer. Gynecol Oncol. 2014;134(3):455-61.

13. Di Donna MC, Cucinella G, Zaccaria G, Lo Re G, Crapanzano A, Salerno S et al. Concordance of Radiological, Laparoscopic and Laparotomic Scoring to Predict Complete Cytoreduction in Women with Advanced Ovarian Cancer. Cancers (Basel). 2023;15(2):500.

14. Aletti GD, Dowdy SC, Podratz KC, Cliby WA. Relationship among surgical complexity, short-term morbidity, and overall survival in primary surgery for advanced ovarian cancer. Am J Obstet Gynecol. 2007;197(6):676.e1-7.

15. Llueca A, Climent MT, Escrig J, Carrasco P, Serra A; MUAPOS working group (Multidisciplinary Unit of Abdominal Pelvic Oncology Surgery). Validation of three predictive models for suboptimal cytoreductive surgery in advanced ovarian cancer. Sci Rep. 2021; 11(1):8111.

16. Daix M, Angeles MA, Motton S, Tanguy Le Gac Y, Ferron G et al. Peritoneal cancer index: laparoscopic evaluation of peritoneal carcinomatosis from gynecological origin. Int J Gynecol Cancer. 2022;32(11):1488-1489.