Faculty of Medicine

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Prognostic significance of the HPV status in early stage cervical carcinoma
(Macedonian Academy of Sciences and Arts, 2006-09)
Kubelka-Sabit, Katerina
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Prodanova, Irina
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Yashar, Genghis
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Zografski, George
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Aims: In order to evaluate their prognostic significance, the parameters of the human papilloma virus (HPV) status were correlated to the lympho-nodal and tumor status, maximal diameter, minimal thickness of uninvolved stroma, histologic type, grade of differentiation, lympho-vascular space invasion, degree of lymphocytic inflammatory stromal reaction at the invasion front, age and the disease-free survival (DFS) of the patients with early stage invasive cervical carcinomas. Material and methods: 77 cases of cervical carcinomas, limited to the uterus, surgically treated and postoperatively irradiated, were selected for this retrospective study. HPV DNA status (presence and HPV type, type of hybridization signal and number of positive cells per sample) was evaluated using sensitive in situ hybridization detection kit with catalyzed signal amplification with biotinylated probes for types 6/11, 16/18 and 31/33 or 31/33/51. Results: The presence of HPV DNA was detected in 45 (58.4%) cases. Thirty-two (71.1%) showed positivity for HPV type 16/18, 8 (17.8%) for 31/33, whereas multiple infection was detected in (8.9%) 4 cases. Dot hybridization signal was found in 31 (68.9%), diffuse in 2 (4.4%) and mixed in 12 (26.7%) cases. More than five positive nuclei per sample were found in 37 (82.2%) of the cases. Only the presence of HPV was associated with absence of regional lymph node involvement, presence of moderate/abundant lymphocytic infiltration and longer 5 and 10-year DFS. Conclusions: According to our results, more extensive studies are needed to assess the real prognostic influence of the other parameters of HPV status in early stage cervical carcinomas.
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Small and large cell neuroendocrine carcinomas of the uterine cervix. A report of 10 cases.
(Springer, 2005-08)
Kubelka-Sabit, Katerina
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Plaseska-Karanfilska, Dijana
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Prodanova, Irina
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Yashar, Genghis
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Hadzi-Nicheva, Biljana
BACKGROUND: Small (SCC) and large cell (LCC) neuroendocrine carcinomas of the uterine cervix are rare and highly aggressive neoplasms. Their association with the integration of human papilloma virus (HPV) DNA of the types 16 or 18 has been documented in many studies. AIMS: The purpose of this study is to present the clinical, histopathological, immunohistochemical characteristics and the presence of HPV DNA in ten cases of SCCs and LCCs of the uterine cervix. METHODS: Seven patients with primary SCCs and three patients with LCCs of the uterine cervix were diagnosed at our department between 1989 and 2004. Clinical data were retrieved from the patients’ files and included age, recurrence and survival. Routinely processed operative and/or biopsy specimens were used for immunohistochemical stains and hybridization procedures. Primary antibodies against several epithelial, neuroendocrine, mesenchimal and proliferative markers were included. The presence of HPV DNA was assessed by conventional in situ hybridization (ISH) using probes for HPV 16/18 and 31/33/51 and polymerase chain reaction (PCR), using three primers (MY09/11, GP5+/GP6+, E6). Six of the patients were surgically treated. Postoperatively, four received chemo and/or radiotherapy, two rejected further treatment and one patient was lost to follow-up. The other four patients underwent conservative treatment due to advanced disease. RESULTS: The patients’ age ranged from 25 to 71 years. Histologically, the tumors showed trabecular, nesting or a sheet-like pattern, with areas of necrosis and frequent mitoses. Their neuroendocrine nature was confirmed by diffuse positive immunostaining for neuron-specific enolase and low-molecular weight cytokeratins. Focal positivity for chromogranin, synaptophysin and S100, together with pancytokeratin and EMA, was evident in the majority of the tumors. Their aggressive potential was confirmed by high Ki-67 proliferative index (50-90%). HPV types 16/18 were found in 4 tumors using ISH, and HPV 16 in additional 3, using PCR (type 16). 3 of the patients developed distant metastases and died 7-48 months after receiving partial or full treatment, while 6 are alive and without evidence of disease after 4-38 months. CONCLUSIONS: SCCs and LCCs are highly aggressive neoplasms. However, early diagnosis and combined therapy may improve survival in some patients. Although mainly a morphologic diagnosis, immunohistochemistry may help in the diagnosis of SCC and LCC.
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Ki-67 expression in the invasion front as an additional independent significant prognostic factor influencing reccurence in early stage cervical carcinomas.
(Springer, 2005-08)
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Prodanova, Irina
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Kubelka-Sabit, Katerina
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Yashar, Genghis
INTRODUCTION: The attempts to determine the prognostic significance of biological markers and their relation to human papillomavirus (HPV) infection in cervical cancer have yielded controversial results. AIMS: The aims of this retrospective study were to correlate alterations of cell proliferation, growth, differentiation and apoptosis regulatory proteins in early stage cervical carcinomas with HPV infection, histopathological and clinical parameters, and to estimate their prognostic significance. METHODS: Expression of Ki-67, p53, mdm-2, bcl-2, c-erbB-2, EGFR protein, as well as estrogen and progesterone receptors was evaluated by immunohistochemistry in operative specimens of 83 patients with early stage cervical carcinoma. The results were assessed semiquantitatively in the surface area, center and invasion front of each tumor as a percentage of the immunostained cells and/or intensity of immunostaining for each protein. The presence of HPV was assessed by conventional in situ hybridization (ISH) technique and catalyzed reporter deposition signal amplification ISH using mixed biotinylated probes to identify types 6/11, 16/18 and 31/33 or 31/33/51. RESULTS: In our case series 73 patients had a tumor limited to the uterine cervix less than 4 cm in diameter (pT1b1), while 10 patients had larger neoplasms belonging to pT1b2 category. Pelvic lymph node involvement was found in 20 patients. During the follow-up period (range, 65 -181, mean, 121 months) recurrences were observed in 9 patients. The 5, 10 and 15-year disease-free survival rate was 92.7%, 90.8% and 86.6%, respectively. Among the 18 variables pelvic lymph node involvement (P=0.0008), tumor diameter (P=0.035), depth of stromal invasion (P=0.029), histotype (P=0.0009), grade (P=0.056), HPV DNA presence (P=0.056), HPV type (P=0.043), as well as bcl-2 (P=0.035), mdm-2 (P=0.051), EGFR (P<0.0001), and Ki-67 (P=0.031) expression in the tumor’s invasion front were identified as important predictive indicators of recurrence in the univariate analysis. Independent significant prognostic factors for disease-free survival in multivariate analysis were the histotype, HPV DNA presence and Ki-67 expression. CONCLUSIONS: The invasive front of carcinomas proved to be the most important area for tumor prognosis. In addition to the detection of HPV presence and morphological parameters, Ki-67 evaluation could be used in selecting appropriate therapeutical approaches in patients with early stage cervical cancer.
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Iimmunohistochemical expression of c-erbb-2 in early stage cervical carcinoma: Correlation with human papillomavirus infection and prognosis.
(Springer, 2003-09)
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Yashar, Genghis
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Kubelka-Sabit, Katerina
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Prodanova, Irina
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Zografski, George
Introduction: The attempts to determine the prognostic significance of c-erbB-2 oncoprotein expression (OPE) and its relation to human papillomavirus (HPV) infection in cervical cancer have yielded controversial. The aim of this study was to evaluate the patterns of c-erbB-2 OPE in early stage cervical carcinoma and to assess its prognostic value by exploring its relationships to various clinicopathological characteristics, HPV status and recurrence rate. Materials and methods: Radical hysterectomy specimens from 71 cervical carcinoma patients (pT1b1/1b2) were investigated immunohistochemically for c-erbB-2 presence. The c-erbB-2 score (range: 0-400) was determined in the surface area, center and invasion front of each carcinoma. CARD in situ hybridization was used for HPV detection. Results and conclusion: Strong c-erbB-2 OPE was detected in 21, 20, and 32 cases in the invasion front, center and surface area of the tumor, respectively. There was a significant difference in positive staining rate of c-erbB-2 between squamous cell, mixed carcinomas and adenocarcinomas (23%, 50% vs 83%, p=0.005). C-erbB-2 OPE was significantly higher in carcinomas with abundant than in tumors with less abundant peri-tumoral lymphocytic infiltration (36.5% vs 10.5%, p=0.032). In HPV positive carcinomas (41), c-erbB-2 was detected more frequently in type 31/33 versus type 16/18 lesions (75% vs 18.8%, p=0.002). No association was found between c-erbB-2 expression and recurrence rate, lymph node metastasis or any other clinicopathological variable investigated (age, tumor diameter, depth of invasion, grade, vascular invasion). Therefore, immunostaining for c-erbB-2 is unlikely to be of use as a prognostic indicator in early stage cervical carcinomas, while further study is warranted to examine relationships between HPV infection and c-erbB-2 OPE.
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Determination of estrogen, progesterone receptor and ki-67 immunoreactivity in early stage cervical carcinoma: Association with human papillomavirus infection and prognosis.
(Springer, 2003-09)
Yashar, Genghis
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Prodanova, Irina
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Kubelka-Sabit, Katerina
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Zografski, George
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Introduction: The predictive values of estrogen (ER) and progesterone receptor (PgR) status and cell proliferation kinetics in cervical carcinomas are still unsettled. The purpose of this study was to clarify the associations among ER/PgR status and Ki-67 expression and to determine their relationship to human papillomavirus (HPV) infection, recurrence rate and other clinicopathologic parameters (age, tumor diameter, depth of invasion, histotype, grade, vascular involvement, inflammatory infiltrate, lymph node status) in early stage cervical carcinomas. Materials and methods: ER, PgR and Ki-67 immunostaining was performed in 72 cervical carcinoma radical hysterectomy specimens (pT1b1/pT1b2). ER/PgR staining was scored in a semiquantitative fashion, while to evaluate the cell proliferation, the Ki-67 labelling index (LI) was assessed in the surface area, center and invasion front of each tumor. HPV status was determined by CARD in situ hybridization. Results and conclusion: ER positivity was detected in 11 (15%), while PgR positivity in 14 (20%) carcinomas. ER/PgR values were in correlation with Ki-67 LI in all three tumors' compartments (p<0.01). In contrast to ER/PgR status, Ki-67 LI was strongly associated with HPV infection (p<0.01). No relationship was found between PgR or Ki-67 immunoreactivity and either recurrence rate or any other clinicopathological variable investigated. Nevertheless, reduced ER expression was significantly associated with larger tumor diameter (p=0.04) and poor differentiation (p=0.03), as well as lymphovascular involvement (p=0.04) and lymph node metastases (p=0.02). These results suggest that ER, PgR and Ki-67 expression are closely related to neoplastic cell proliferation, probably induced by HPV infection. Their determination may provide additional prognostic information in early stage cervical carcinomas.
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Ovarian mucinous cystadenoma with murale nodule of poorly differentiated squamous cell carcinoma. Report of a case
(Blackwell Publishing Ltd., 2008-10)
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Prodanova, Irina
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Kubelka-Sabit, Katerina
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Zografski, George
Background. Mural nodules associated with mucinous and serous tumors of the ovary may represent a reactive process, a benign tumor, or a malignant neoplasm. Thus, the prognosis of the ovarian tumor can be dramatically modified by the presence of this nodule. We report the clinicopathologic and immunohistochemical findings of a case of a mural nodule of anaplastic squamous cell carcinoma associated with ovarian mucinous cystic tumor. Case report. The patient was a 66-year-old postmenopausal woman (gravida 1, para 1) with a 6-month history of increasing abdominal fullness. An abdominal ultrasound revealed a multilocular left ovarian cyst with a solid component. After total abdominal hysterectomy and bilateral salpingo-oophorectomy, the diagnosis of a mucinous cystadenoma with a focus of FIGO stage IC anaplastic carcinoma in the left ovary was made. The patient received six courses of chemotherapy; 3 months after completing chemotherapy, she developed rectosygmoidal wall metastases. Despite rectosygmoid resection and additional chemotherapy and radiotherapy, the disease persisted in the pelvis and the patient died 14 months after initial operation. The primary tumor nodule as well as metastatic rectosygmoid tumors were studied by conventional and immunohistochemical methods. Results. The left ovarian tumor measured 8.5 x 8 x 6 cm. On cut sectioning, it was multilocular with a solid 4.5 x 4 x 3 cm mural nodule. Microscopically, the cyst wall was predominantly lined with benign mucinous epithelium, with rare foci of endometriosis found in smaller locules. The solid area of the mural nodule showed nests of spindle or polygonal highly malignant cells with admixed inflammatory cells. Necrosis and hemorrhage were also present. The ovarian capsule was invaded by the pleomorphic tumor cells. In favor of a diagnosis of anaplastic carcinoma were poor circumscription of the nodule with lymph-vascular involvement and absence of a prominent inflammatory reaction with multinucleated giant cells of the epulis type. In addition, the metastatic rectosygmoid tumor showed poorly differentiated squamous cell carcinomatous features. Immunohistochemically, the atypical cells of the nodule as well as a metastatic tumor were uniformly positive for epithelial markers such as pan-cytokeratin, high-molecular weight cytokeratin, cytokeratin 7 and epithelial membrane antigen, negative for carcinoembryonic antigen and focally weakly positive for vimentin. Many of these cells were also immunoreactive for p53 (80-90%) and Ki-67 (40-50%). Conclusion. The occurrence of ovarian mucinous cystic tumor with mural nodule of poorly differentiated squamous cell carcinoma is evidently very uncommon, because we have not found a similar case in the literature. The malignant nodules composed of sarcoma or anaplastic carcinoma such as in our case are associated with an unfavourable outcome and must be distinguished from other sarcoma-like nodules that may also occur in the wall of mucinous ovarian tumours. Therefore, the implementation of strict morphologic criteria supplemented by immunohistochemistry aids in the sometimes difficult differential diagnosis among these types of mural nodules.
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Malignant perivascular epithelioid cell tumor of the uterus with aggressive behaviour: A case report
(Blackwell Publishing Ltd., 2008-10)
Prodanova, Irina
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Kubelka-Sabit, Katerina
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Background. The perivascular epithelioid cell tumor (PEComa) is recognized by the World Health Organization as a mesenchymal neoplasm showing at least partial morphological and immunohistochemical evidence of a putative perivascular epithelioid cell differentiation. This family of tumors includes angiomyolipoma (AML), lymphangioleiomyomatosis (LAM), clear cell sugar tumor of the lung and distinctive clear cell tumors at various other anatomic sites. Occasionally, PEComas are associated with the tuberous sclerosis complex (TSC). Because non-AML/non-LAM PEComas are extremely rare and their nature and prognostic factors undefined, we present a case of uterine PEComa with obviously aggressive behavior. Case report. A 55-year-old (gravida-2, para-2) presented with a large uterine mass palpated during a routine gynaecological examination. The patient did not have any stigmata or family history of TSC, and had no history of melanoma. A transvaginal ultrasound revealed an enlarged uterus with a heterogeneous mass which size was estimated at 9 x 9 cm. The clinical impression of the lesion was a leiomyoma. Total abdominal hysterectomy with bilateral salpingo-oophorectomy and omentectomy was performed 9 months later, and the pathohistological diagnosis was malignant PEComa of the uterus with metastases in the omentum. Three months after the surgical intervention the patient is still receiving adjuvant chemotherapy and there is no evidence of recurrence. Results. The uterine body was enlarged and measured 12 x 14 x 8 cm, with lobulated surface. Within the myometrium there was a poorly demarked gray-ten nodular tumor occupying the fundus, anterior and posterior walls with focally hemorrhagic areas and necrosis on cut surface. The largest diameter of the tumor was 14 cm. In the adipose tissue of the omentum there were numerous nodular tumor masses whose diameters ranged from 1 to 3 cm. Histologically, the tumor demonstrated a tongue-like growth pattern and was composed of large epithelioid cells with clear or eosinophilic cytoplasm, partially arranged around blood vessels The nuclei were mainly round, centrally located, and vesicular, with moderate to severe pleomorphism and hyperchromatism. Extensive cellular atypia, including bizarre multinucleated giant cells with large nuclei and nucleoli, was present as well. Mitotic count was high (15 per 50 HPFs), with prominent coagulative tumor necrosis. The microscopic examination of the nodular tumors from the omentum exhibited the same morphological features. Immunohistochemically, the tumor cells showed positivity for HMB-45 and smooth muscle actin while they were negative for cytokeratins, carcinoembryonic antigen, S-100 protein, CD-10, caldesmon and desmin. Immunoreactivity for vimentin was inconspicuous. The estrogen and progesterone receptors were also negative. A proliferative index of 30% was noted with Ki-67 immunostaining. The morphology and immunohistochemical profile of the lesions was consistent with PEComa. Conclusion. Due to the fact that a vast majority of PEComas has a benign course of disease or is considered to be of uncertain malignant potential, we present this case with evident aggressive behaviour since we believe that the histological features of this tumor can serve as a model for defining of the criteria for potentially malignant PEComas.
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Immunohistochemical expression and prognostic significance of DCC (deleted in colon cancer), p53 protein and proliferative marker Ki-67 in colorectal colon cancer.
(Springer, 2005-05)
Yashar, Genghis
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Prodanova, Irina
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Kubelka-Sabit, Katerina
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Objectives: The objective of this study was to evaluate the immunohistochemical expression of Deleted in colon cancer (DCC), p53 protein and proliferating index Ki-67 in correlation with various clinico-pathological (age, sex, tumor status, lymph node involvement, localization, tumor diameter, grade of differentiation, histological type) and biomolecular parameters (loss of heterozygosity of the long arm of chromosome 18 and microsatellite instability) in colorectal cancer patients. In addition, the prognostic significance of their influence on overall survival (OS) was also estimated. Methods: A retrospective analysis of 100 patients with colorectal cancer who underwent large bowel resection with regional lymphadenectomy was conducted in the period between 1995 and 2000. All the patients were in stage II and stage III of the disease according to the postoperative TNM classification of UICC (1997) guidelines. The immunohistochemical expression of protein products of the DCC, p53 tumor suppressor genes and Ki-67 proliferating index were semi-quantitatively evaluated. Biomolecular analyses for the loss of heterozygosity of the chromosome 18q and microsatellite instability were performed with the Polymerase chain reaction (PCR) technique. Results: In our case series, 57 (57%) patients were in stage II, and the remaining 43 (43%) patients in stage III of the disease. During the follow-up period (mean 53, range 5-97 months), 41(41%) patients died of the disease. The expected 5-year OS rate was 58.6%. In the univariate analysis, tumor status, lymph node involvement, sex, age, tumor grade, p53 protein expression and Ki-67 proliferating index were parameters with prognostic significance related to OS (p<0.05). Among these variables, in the multivariate analysis the tumor status and Ki-67 proliferating index were selected as independent and significant prognostic factors related to OS (p=0.0019). According to the value of the prognostic index (PI) defined by Cox regression model, the patients were categorized in two distinct risk groups. The 5-year OS rate of the low- and high-risk group patients was 65.0% vs. 29.4% (p=0.001). The 5-year OS for stage II was 71.1% vs. 40.0% (p=0.05) and for stage III of the disease it was 54.8% vs. 25.0% (p=0.03), respectively. Conclusions: These data indicate that defining prognostic groups in each stage of the disease allow an exact and objective selection of colorectal cancer patients with different death risk. Therefore, the prognostic index (PI) as an indicator of the patient’s place in the prognostic spectrum could be a sound basis for an appropriate planning.
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Ovarian cellular fibromas: A cliniopathological and immunohistochemical analysis of 10 cases.
(Springer, 2007-08)
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Prodanova, Irina
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Kubelka-Sabit, Katerina
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Zografski, George
BACKGROUND: Traditionally, cellular fibroblastic tumors of the ovary were classified as either cellular fibroma (CF) or fibrosarcoma. A recent study suggests that cellular fibromatous neoplasms with bland cytology and elevated mitotic counts are associated with favourable prognosis and should be diagnosed as "mitotically active cellular fibroma" (MACF) rather than fibrosarcoma. In addition to clinicopathological features, immunohistochemistry may aid in further differentiating between CF and MACF, but its role has not been analyzed so far. METHOD: We retrospectively analyzed the clinicopathological and immunohistochemical features of 10 cases of ovarian cellular fibroblastic tumors diagnosed either as CF or fibrosarcoma in the last seven years. Patient records and archival pathology specimens were reviewed and immunohistochemistry was performed using pan-cytokeratin, EMA, vimentin, inhibin-alpha, calretinin, CD10, CD99, alpha-smooth muscle actin (SMA), desmin, S-100, c-kit, estrogen (ER), progesterone receptor (PR), p53, bcl-2, and MIB-1 antibody. RESULTS: Utilizing criteria proposed by Irving et al. the tumors were reclassified as CF (0-3 MFs/10 HPFs, n=5) and MACF (>4 MFs/10 HPFs, n=5). The mean age of patients with CF and MACF was 44 and 36 years, respectively. All tumors were unilateral, and the mean tumor size of CFs was 6.0 cm and 13.3 cm for MACFs. The majority of the tumors were solid; four of them had a cystic component, while ovarian surface rupture was present in one CF and one MACF. All tumors consisted of cellular, intersecting bundles of spindle cells showing slight or moderate pleomorphism. The mean highest mitotic count was 2.3 MFs/10 HPFs for CF, and 7.6 MFs/10 HPFs for MACFs. Follow-up of 4 to 79 months (mean 38 months) was available in 9 patients and was uneventful in all cases. One patient with MACF died 15 days following the operation as a result of the intercurrent disease. Immunohistochemical analyses showed that spindle cells in majority of the tumors were immunoreactive for vimentin, alpha-SMA, inhibin-alpha, calretinin, PR, and bcl-2. All tumors were negative for pan-cytokeratin, EMA, CD10, CD99, c-kit, ER, and p53, while one CF was positive for S-100, and one MACF showed positivity for desmin. In addition, the MIB-1 labeling index (LI) in MACFs was higher (mean 14.4%, range 10-25%), than that in CF (mean 5.6%, range 3-10%). CONCLUSION: Our results confirm the immunophenotypic similarity between ovarian fibromas and cellular fibromatous neoplasms, and suggest that the use of MIB-1 LI may help in differentiating between CF and MAFC.
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Evaluation of combined bcl-2/mdm-2 immunohistochemical expression as a prognostic factor in early stages of invasive cervical carcinomas
(Springer, 2007-08)
Prodanova, Irina
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Kubelka-Sabit, Katerina
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BACKGROUND: The present study was designed to evaluate the immunohistochemical expression of apoptosis regulating proteins (bcl-2, mdm-2 and p53) in correlation with proliferation (Ki-67), human papillomavirus (HPV) infection and other histopathological and clinical parameters in early stage cervical carcinomas and the estimation of their prognostic significance. Special attention was given to combined bcl-2/mdm-2 immunophenotypes in predicting the recurrence of the disease. METHOD: The subject of this study was a series of 83 surgically treated patients with cervical carcinoma confined to the uterine cervix (pT1b1/1b2), who subsequently received complete radiotherapy. The presence of HPV DNA was determined by the conventional method of in situ hybridization (ISH) and catalyzed reporter deposition signal amplification ISH. The immunostaining was performed using avidin-biotin-peroxidase complex method and the expression of the biological markers was semiquantitatively evaluated as the percentage of immunostained cells. RESULTS: During the clinical follow-up (mean 120.7, range 4.4-181 months) a relapse was diagnosed in 9 (10.8%) patients and the expected 5-, 10- and 15- year disease-free survival was 92.7%, 90.8% and 86.6%, respectively. The results of the univariate analysis indicate that significant predictive indicators for recurrence are: lymphonodal status, maximal tumor diameter, depth of stromal invasion, histological type and HPV DNA presence and type. Immunohistochemical markers showed the following correlations: increased expression of Ki-67 (P=0.031) and bcl-2 negativity (P=0.047) correlated with poor disease-free survival, while mdm-2 positivity showed borderline significance (P=0.051) and p53 expression had no influence on disease-free survival. Additional evaluation of combined bcl-2/mdm-2 expression showed that cases with bcl-2+/mdm-2- and bcl-2-/mdm-2+ immunophenotype had better survival (P=0.048) compared to bcl-2+/mdm-2+ and bcl-2-/mdm-2- phenotype. In the multivariate analysis, histological type, HPV DNA presence and the expression of Ki-67 have been selected as the most significant independent prognostic parameters (P=0.0024). CONCLUSION: The evaluation of combined bcl-2/mdm-2 immunohistochemical expression provides more relevant information for the prediction of the recurrence of the disease than their individual expression. However, neither individual expression of bcl-2 and mdm-2 nor their combined immunohistochemical expressions are independent predictors of prognosis in early stages of invasive cervical carcinomas.

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