INTRODUCTION Ovarian cancer is the leading cause of mortality from gynecologic malignancies in the industrialized countries and is responsible for

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1 INTRODUCTION Ovarian cancer is the leading cause of mortality from gynecologic malignancies in the industrialized countries and is responsible for more deaths than both cervical and endometrial tumours. The tumour biology of epithelial ovarian cancer differs from that of most other epithelial tumours, because of the intraperitoneal spreading leading to exfoliation of cancer cells into the peritoneal fluid. The prognostic factors can be used to predict the future course of the malignancy and may identify a subgroup of patients with high-risk disease. The prognostic factors of ovarian tumours can be classified into clinico-pathological and molecular markers. Clinico-pathological factors include patient-, tumour- and therapy-related characteristics. For prognostic purposes more and more molecular markers are are currently under evaluation to define the category of risk to which an individual patient can be assigned. Six different groups of molecular markers are known. Developments in molecular techniques have resulted this new generation of prognostic factors. In my thesis, I deal separately with the molecular and clinico-pathological prognostic factors. To estimatate the future course of ovarian carcinoma and to optimize the most appropriate treatment, the knowledge of different prognostic factors is essential. In my thesis I examined the following clinico-pathological factors: Ovarian cancer may occur at any age but is most common between years of age. Patients younger than 60 usually have better prognosis than patients older than 60. The stage of the tumour is the most important prognostical factor. The relationship between the histology and the prognosis is not unambiguos. The most common - serous - tumours are usually considered to be agressive, as opposed to endomerioid and mucinous tumours. Clear-cell carcinomas are also thought to be agressive. The classification of the degree of differentation of ovarian carcinoma is based on the Federation International d Gynecology et Obstetrique (FIGO), the Gynecology Oncology Group (GOG) and the World Health Organization (WHO). However, these grading systems are not perfect, but grading is considered to be a prognostic factor. Ascites or tumour cells in peritoneal washing are adverse prognostic factors. The residual tumour volume and the employed surgical procedure are the most important treatment related prognostic factors.

2 In my thesis, I examined two members of the metastasis-cascade. First, I analyzed fibronectin which is an adhesion molecule and may have an important prognostic role in ovarian cancer. The second examined molecular marker was the matrix metalloproteinase-2/9, which belongs to proteolytic enzymes produced by both connective tissue and tumour cells and could degrade components of the the extracellular matrix (ECM). Of special importance to epithelial ovarian cancer spread are the type IV gelatinases, Mr 72,000 (MMP-2, gelatinase A) and Mr 92,000 (MMP-9, gelatinase B) enzymes, because of their preference to degrade type IV collagen which is the major component of basement membranes. This degradation is an essential step in tumour invasion. There is evidence from studies with epithelial ovarian cancer that MMP-2 and MMP-9 activity play an important role in the invasion and metastasis of epithelial ovarian cancer. There is evidence from studies with ovarian cancer cell lines that fibronectin activates MMP-9 secretion via the MEK1-MAPK and the PI3K-Akt pathways in ovarian cancer cells. Fibronectin produced by mesothel cells of the peritoneum stimulates MMP-9 expression of ovarian cancer cells and thus probably invasion and dissemination. Fibronectin was identified in ascites of advanced ovarian cancer patients. Cancer cells are transformed cells in which DNA-synthesis is considerably elevated compared to that of normal cells. There are high activities of purine and pyrimidine biosynthetic enzymes involving both de novo and salvage biosynthetic pathways. The most important enzyme in the de novo biosynthetic pathyway is the ribonucleotid reductase. However, most tissue can synthesize both purine and pyrimidine in the salvage pathway. In this respect, pyrimidine synthesis may continue through both the de novo pathway, in which the key enzyme is the thymidylate synthase (TS) and through the salvage pathway in which the key enzyme is the thymidine kinase (TK). Both enzyme s activities lead to production of thymidine-three phosphate. Thymidine kinase is located in the cytoplasm and its activity depends on the cell cycle, because in the S-phase, the TK activity is ten times higher than in the G1-phase. The DNA-synthesis through the salvage pathway in tumour cells may continue even if the de novo pathway is blocked. This indicates that pyrimidine synthesis may continue through both the de novo pathway, where the key enzyme is the thymidylate synthase (TS) and through the salvage pathway where the key enzyme is the thymidine kinase (TK).

3 OBJECTIVES I chose the topic because I have several times seen that the outcome of apparently similar cases of epithelial ovarian cancers is highly variable, and the traditional prognostic factors often would not predict disease outcome in a clinically useful manner. To examine this problem I analyzed in detail the following topics: 1. To examine the survival and clinico-pathological prognostic factors of patients treated at the 1 st. Department of Obsterics and Gynecology Semmelweis University Faculty of Medicine between Are these prognostic factors useful to predict disease outcome and survival of ovarian malignancies? 2. To compare the survival with the similar data of the twenty-fifth Annual Report on the Results of Treatment in Gynecological Cancer of FIGO in order to evaluate the efficiency of the treatment. 3. To analyze the prevalence, clinical course and molecular markers of ovarian tumours of low malignant potential (LMP). To review our experience with the fertility-sparing surgery in the treatment of LMP ovarian tumours of patients younger than To assess the prognostic value of MMP-2 and MMP-9 activities and fibronectin expression in ovarian cancer patients. 5. To compare the usefulness of traditional clinico-pathological prognostic factors to the examined molecular markers during the disease course. 6. To examine the activity and thermostability one of the key enzymes of the salvage DNA-synthesis in ovarian cancer and in normal ovaries. To fulfill these objectives I employed experimental and mathematical-statistical methods. MATERIAL AND METHODS Between 1993 and 2003, 155 patients with epithelial ovarian carcinomas and 47 patients with ovarian tumours of low malignant potential had been treated at the 1 st. Department of Obsterics and Gynecology Semmelweis University Faculty of Medicine. Those patients who have previous underwent chemotherapy or radiation therapy were excluded from the study. Collaborative research was started in 2002 between the oncological division of the I st. Department of Obstetrics and Gynecology and I st. Department of Pathology and Experimental Cancer Research of Semmelweis University. We asked for and received permission from the Regional and Institutional Committee of Science and Research Ethics of Semmleweis University. The goal was to investigate the relationship between the course of ovarian carcinoma to the mutual effect on the tumor cells and extracellular matrix. I examined the role

4 of molecular markers in the prognosis of ovarian tumours by employing molecular pathological procedures. The samples were collected from the operating rooms of the I st. Department of Obstetrics and Gynecology. The prognosis of epithelial ovarian cancer is considered better in young patients. To test this theory, I divided the patients into two groups according to their age. Those patients who were younger than 60 years of age at the time of diagnosis created the first group and those who were older created the second group. Comprehensive surgical staging was done based on the FIGO-classification. The histological examination was performed in the Histopathological Laboratory of the I st Department of Gynecology and Obstetrics. In cases where the tumour was questionable, a second-opinion was asked from either the I st Department of Pathology and Experimental Cancer Research or from the Oncopathological Laboratory of the National Oncological Institute. Samples were collected from ascites in every case and the volume was measured. If the volume was greater than 1000 ml, it was considered and classified as large quantity. Based on the measured diameter of residual tumor mass, the surgical procedure was considered optimal if it was less than 1 cm, otherwise it was considered suboptimal. I analyzed the role of prognostic factors in the patient survival rate. I also examined the possibility of employing fertility-sparing surgery in the treatment of borderline ovarian tumours. For those patients with low malignancy ovarian tumours who were older than 40, transabdominal hysterectomy and bilateral salpingoophorectomy was offered. I compared the survival with the similar data of the twenty-fifth Annual Report on the Results of Treatment in Gynecological Cancer of FIGO in order to evaluate the efficacy of the treatment. In order to investigate tumours with molecular markers, the serum and ascites of 22 patients with histologically verified ovarian tumours were analyzed. In the serum and ascites, matriolytic activity was detected in the surgically removed tumours by means of gelatin zymography. The samples were transported into the pathological laboratory under 4 C, where it was pulverized in the mortar and frozen immediately in liquid nitrogen. Proteolysis was detected as a white zone in a dark field and quantitative assessment was performed by using densitometric scanning with an Eagle Eye II (Stratagene, CA, USA). Each gel was scanned twice, and a standard curve was set up for every zymogram in relation to the gelatinolytic activity of recombinant MMP-2 and MMP-9. MMP-2 and MMP-9

5 gelatinolytic activity present in the ovarian tissues was compared with this curve. MMP-2 and MMP-9 activity was expressed in arbitrary units (U) per microgram of ovarian cancer tissue. Fibronectin content was identified by immunotechnique blot analysis and its quantity was estimated by densitometer analysis. The fibronectin concentration was determined using densitometric scanning with an Eagle Eye II, taking into account the intensity and the width of the band. Each gel was scanned twice, and a standard curve set up for every zymogram in relation to the fibronectin expression present in the ovarian tissues was compared with this curve. Fibronectin concentration was expressed in arbitrary units (U) per microgram of ovarian cancer tissue. The results were correlated to the clinico-pathological parameters, disease recurrence and patient survival, with a median follow-up period of 30 months. Thymidine kinase activity ( 14 C TdR + ATP TK 14 C-dTMP + ADP) was measured by the PEI cellulose plate method. TK activity was calculated in nmol substrate metabolised per hour per mg protein. Because of our interest to analyze thermostablity of TK, samples were incubated at 37 o C for three hours and TK activity measured every l5 minutes. We calculated the percent of TK activity in the presence of ATP and CTP, and estimated the relative contributions of TK isoenzymes to total TK activity in 7 ovarian cancers and in 9 normal ovaries. Statistical Analysis Different biostatistical methods were employed to analyze the data. Survival data was calculated begining the date of surgery. Treatment and survival data were supplemented from medical record reviews and from the Population Register Office. In order to compare different prognostic factors, a multvariate Cox proportional regression analysis was performed. A p value of <0.05 was considered to be significant. To compare activity of thymidine kinase, Student s t test was employed. Variances between MMP-2/9 activities and fibronectin expression were analyzed with ANOVA and differences between groups were evaluated using Student s t test. A p value of <0.05 was considered to be significant. RESULTS The morbidity of epithelial ovarian cancer increases with age. The most affected age group was between years of age in regard to carcinoma and between years in regard to

6 borderline tumours. The number of cancer patients with stage I and stage II tumors is about the same, however, 79% of patients were diagnosed in stage III. Disseminated malignancy was verified in about 10% of the patients. Approximately two thirds of the carcinomas were of serous histology. Surprisingly, most carcinomas were anaplastic. Ascites was presented in almost all patients with carcinoma and the volume of the ascites correlated to the stage of the disease. Optimal surgical procedure was done in more than half of the patients, however in 13% of the patients, only explorative laparotomy could be done. Twenty-eight percent of the patients with borderline ovarian tumours were younger than 40. Of them, 10 patients who wished to have children underwent fertility-sparing surgery. Half of them became pregnant and had healthy children. The 5-year survival of ovarian tumours with low malignant potential was 90%, and of epithelial ovarian cancers was 30,9%, respectively. Multivariate analysis identified adverse prognostic factors, including advanced age (>60 years) and stage, high grade and suboptimal operation with residual macroscopic disease and the presence of ascites. By examining the Kaplar-Meier-curves, the adverse survival was most strongly influenced by advanced stage. The relationship between the survival and age showed that those patients who were 60 years or older had twice the risk of dying from ovarian cancer compared to those who were younger. Histological type was not identified to be an adverse prognostic factor in this study, however mucinous and clear-cell types had a more favourable prognosis than serous types. Poorly differentiated carcinomas were associated with significantly decreased survival, since the mean survival time was approximately six times shorter for ovarian cancer patients with anaplastic tumours. There was no significant difference in regard to survival between well and moderately differentiated carcinomas. The patients whose carcinomas lacked ascites showed a survival time twice as long as those with ascites. In those patients who had more than 1000 ml ascites, the 5-year survival was less than 10%. The second strongest predictor of survival was the type of surgical procedure and the measured diameter of the residual tumour volume. The 5-year survival of patients who had an optimal operation was approximately ten times higher than patients who had a suboptimal operation.

7 No correlation could be seen between the histology of the ovarian tumours and the elevation of MMP-2/9 activity and fibronectin expression. I did not measured MMP-2/9 activity in normal ovaries, however I did find MMP-2/9 activity in ovarian tumours. Although the fibronectin concentration was particularly elevated in epithelial ovarian cancers, there was no statistically significant difference between fibronectin concentration in benign, borderline, and malignant ovarian tumours. Fibronectin expression was lower in early stage carcinomas compared to advanced stage tumours. However, the fibronectin concentration was significantly higher in patients who died because of ovarian cancer. The significantly elevated MMP-9 activity in ovarian cancer patients with recurrence may improve the theory that MMP-9 as opposed to MMP-2 is important not only in proliferation but also the dissemination of epithelial ovarian cancer. It is also possible that those ovarian cancer cells which have higher MMP-9 activity and fibronectin concentration may be more resistant to chemotherapy. There was no differences between the clinical-pathological parameters of recurrent and non-recurrent ovarian cancers. However, expression of MMP-9 and fibronectin concentration in recurrent ovarian cancer patients was significantly higher. In addition, the fibronectin concentration in the serum and ascites of recurrent ovarian cancer patients was also higher, though not significantly. MMP-9 activities in the serum and ascites of recurrent ovarian carcinomas were also higher, but only the MMP-9 activity elevation in the ascites was significant. MMP-2 activity was moderately but not significantly higher in recurrent ovarian carcinomas. Thymidine kinase activity was significantly higher in ovarian carcinoma extracts in contrast to normal ovaries, indicating elevated proliferation and mitotic activity. Thymidine kinase-2 isoenzyme can also be found in normal ovaries, which is produced by mitochondria and is more stable to thermal activity. The thymidine kinase-1 isoenzyme, which is found predominantly in the cytosol, is capable of dividing cells such as ovarian carcinoma cells and is thermally unstable and more subject to inactivation by thermal effect than the normal ovarian extracts. The TK-2 isoenzyme could usually only be revealed in the S-phase. I have found a notable difference between the thermostability of TK isoenzymes, which indicates clearly their different characteristics. CONCLUSIONS Oldaltörés 1. Multivariate analysis identified adverse prognostic factors including advanced age

8 (>60 years) and stage, high grade and suboptimal operation with residual macroscopic disease, and the presence of ascites. However, the histological type was not identified to be an adverse prognostic factor in this study. 2. The 5-year survival of patients with early stage ovarian carcinoma at Semmelweis University s 1 st Department of Obstetrics and Gynecology is similar to the survival of patients in the twenty-fifth Annual Report on the Results of Treatment in Gynecological Cancer of FIGO. However, 5-year survival for advanced stage ovarian cancer patients in 1 st Dept. of Obstetrics and Gynecology of Semmelweis University is 6% lower in regard to stage III carcinomas, and 13% lower in respect to stage IV carcinoma patients respectively. The reason may be that taxol treatment had been introduced later in the chemotherapy of ovarian cancer in Hungary than most countries in the FIGO-survey. 3. The prevalence, clinical course, and recovery of ovarian tumour patients with low malignant potential at the 1 st Dept. of Obstetrics and Gynecology of Semmelweis University was similar to patients of the twenty-fifth Annual Report on the Results of Treatment in Gynecological Cancer of FIGO. The fertility-sparing surgical procedure should be offered to young patients with early stage, low malignant potential ovarian tumours. In this study, half of those patients who had undergone fertility-sparing surgical procedure became pregnant and had a healthy newborn. 4. No correlation could be seen between the histology of the ovarian tumours and the elevation of MMP-2/9 activity and fibronectin expression. There was no statistically significant difference between MMP-2/9 activity and fibronectin concentration in ovarian carcinomas compared to normal ovaries so these molecular factors are not candidate markers for screening of ovarian carcinomas. 5. I previously stated that activated forms of MMP-9, MMP-2, and fibronectin concentration corresponded with the clinical course of epithelial ovarian carcinomas. The expression of these molecular markers in recurrent ovarian carcinomas was significantly higher compared to ovarian cancers without recurrence. MMP-9 activity and fibronectin concentration could be an appropriate molecular markers which may point out the high-risk subtype of epithelial ovarian carcinoma. 6. Thymidine kinas-1 isoenzyme activity was significantly higher in ovarian carcinoma extracts than in normal ovaries, indicating elevated proliferation and mitotic activity in the S-phase. Thymidine kinase is a potentially promising goal to the enzyme-pattern targeted chemotherapy

9 Oldaltörés

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