Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi

Nazlı Topfedaisi Özkan; Nezaket Kadıoğlu; Burcu Timur; Mehmet Mutlu Meydanlı

doi:10.37989/gumussagbil.1049371

Araştırma Makalesi

The Relationship between Plasma D-Dimer Level and Prognostic Factors in Cases with High-Grade Serous Ovarian Cancer

Yıl 2022, Cilt: 11 Sayı: 1, 153 - 157, 19.03.2022

Nazlı Topfedaisi Özkan Nezaket Kadıoğlu Burcu Timur Mehmet Mutlu Meydanlı

https://doi.org/10.37989/gumussagbil.1049371

Öz

Ovarian cancer is the leading cause of cancer-related death among gynecological cancers. Hypercoagulation and fibrinolysis increase due to hemostatic activation are frequently observed in advanced stages. We aimed to examine the clinical prognostic value of plasma D-dimer levels measured before the operation in high-stage serous ovarian cancer cases. We conducted a retrospective analysis of 142 patients who had diagnosed with high-grade serous ovarian cancer (HGSC) between 2013-2017 at the Gynecological Oncology Clinic of Dr.Zekai Tahir Burak Training Hospital. Age at diagnosis, pre-treatment plasma D-dimer level, presence of ascites, residual tumor, CA125 level, FIGO stage, and other demographic information were obtained. The mean patient age was 55.25 ±10.84 year. The D-dimer level was normal in 52 (%36,6) patients and high in 90(%63,4) patients. While there was no significant difference when the age limit of 60 was taken in cases with and without high D-dimer levels. Patients with FIGO stage(III-IV) was higher in cases with high D-dimer levels(p<0.001), the presence of massive ascites(p<0.001) and residual tumor. was found to be more likely to occur with high D-dimer levels(p<0.001). A positive correlation has been shown between the cytokines related to tumor burden and angiogenesis, interleukin 6, serum vascular endothelial growth factor (SVEGF), platelet vascular endothelial growth factor (PDEGF) and plasma D-dimer level in previous studies and more evidence suggests the existence of a correlation between coagulation activation and fibrinolysis and tumor angiogenesis, invasion, progression, and metastatic spread. According to the results of our study, high plasma D-dimer levels in HGSK patients seem to be associated with advanced disease and high residual disease burden. Since it is an easily measurable parameter, it suggests that it is a marker that can be used in clinical practice.

Anahtar Kelimeler

D-dimer levels, high grade serous ovarian cancer, hypercoagulation, fibrinoliysis

Kaynakça

1. Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., Parkin, D. M., Forman, D. and Bray, F. (2015). “Cancer Incidence and Mortality Worldwide: Sources, Methods and Major Patterns in GLOBOCAN 2012.” International Journal of Cancer, 136(5), E359-86. https://doi.org/10.1002/ijc.29210
2. Kurman, R. J. and Shih, I.-M. (2016). “The Dualistic Model of Ovarian Carcinogenesis: Revisited, Revised, and Expanded.” The American Journal of Pathology, 186(4), 733–747. https://doi.org/10.1016/j.ajpath.2015. 11.011
3. Koshiyama, M., Matsumura, N. and Konishi, I. (2017). “Subtypes of Ovarian Cancer and Ovarian Cancer Screening.” Diagnostics (Basel, Switzerland), 7(1), 1-5. https://doi.org/10.3390/diagnostics7010012
4. Cooke, S. L., & Brenton, J. D. (2011). “Evolution of platinum resistance in high-grade serous ovarian cancer”. The Lancet. Oncology, 12(12), 1169–1174. https://doi.org/10.1016/S1470-2045(11)70123-1
5. Ogata, Y., Heppelmann, C. J., Heppelmann, C. J., Charlesworth, M. C., Madden, B. J., Miller, M. N., Kalli, K. R., Cliby, W. A., Bergen, H. R., Saggese, D. A. and Muddiman, D. C. (2006). “Elevated Levels of Phosphorylated Fibrinogen-Alpha-Isoforms and Differential Expression of Other Post-Translationally Modified Proteins in The Plasma of Ovarian Cancer Patients.” Journal of Proteome Research, 5(12), 3318-3325. https://doi.org/10.1021/pr060344+
6. Ogata, Y., Heppelmann, C. J., Heppelmann, C. J., Charlesworth, M. C., Madden, B. J., Miller, M. N., Kalli, K. R., Cliby, W. A., Bergen, H. R., Saggese, D. A. and Muddiman, D. C. (2006). “Elevated Levels of Phosphorylated Fibrinogen-Alpha-Isoforms and Differential Expression of Other Post-Translationally Modified Proteins in The Plasma of Ovarian Cancer Patients.” Journal of Proteome Research, 5(12), 3318-3325. https://doi.org/10.1021/pr060344+
7. Miralles, C., Orea, M., España, P., Provencio, M., Sánchez, A., Cantos, B., Cubedo, R., Carcereny, E., Bonilla, F. and Gea, T. (2003). “Cancer Antigen 125 Associated with Multiple Benign and Malignant Pathologies.” Annals of Surgical Oncology, 10(2), 150–154. https://doi.org/10.1245/aso.2003.05.015
8. Sakurai, M., Matsumoto, K., Gosho, M., Sakata, A., Hosokawa, Y., Tenjimbayashi, Y., Katoh, T., Shikama, A., Komiya, H., Michikami, H., Tasaka, N., Akiyama-Abe, A., Nakao, S., Ochi, H., Onuki, M., Minaguchi, T., Yoshikawa, H. and Satoh, T. (2017). “Expression of Tissue Factor in Epithelial Ovarian Carcinoma Is Involved in the Development of Venous Thromboembolism.” International Journal of Gynecological Cancer : Official Journal of the International Gynecological Cancer Society, 27(1), 37-43. https://doi.org/10.1097/IGC.0000000000000848
9. Varol A, Köktürk N, Kılıç H, Aydoğdu M, Ekim NN. (2012). “The Role of Quantitative D-Dimer Levels in The Follow-Up and Differential Diagnosis of Pulmonary Thromboembolism and Community- Acquired Pneumonia.” Turk J Med Sci, 42, 639-47.
10. Lin, Y., Liu, Z., Qiu, Y., Zhang, J., Wu, H., Liang, R., Chen, G., Qin, G., Li, Y. and Zou, D. (2018). “Clinical Significance of Plasma D-Dimer And Fibrinogen in Digestive Cancer: A Systematic Review and Meta-Analysis.” European Journal of Surgical Oncology : The Journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology, 44(10), 1494-1503. https://doi.org/10.1016/j.ejso.2018.07.052
11. Zhu, L, Liu, B., Zhao, Y., Liu, L., Yang, C., Yang, Y. and Zhong, H. (2014). “High Levels of D-Dimer Correlated with Disease Status and Poor Prognosis of Inoperable Metastatic Colorectal Cancer Patients Treated with Bevacizumab.” J Cancer Res Ther, 10, 246-51.
12. Chen, L., Wang, X., Shu, J., Xu, S., Wu, Q. and Yu, Y. (2019). “Diagnostic Value of Serum D-Dimer, CA125, and Neutrophil-To-Lymphocyte Ratio in Differentiating Ovarian Cancer and Endometriosis.” International Journal of Gynaecology and Obstetrics: The Official Organ of the International Federation of Gynaecology and Obstetrics, 147(2), 212–218. https://doi.org/10.1002/ijgo.12949
13. Sakurai, M., Satoh, T., Matsumoto, K., Michikami, H., Nakamura, Y., Nakao, S., Ochi, H., Onuki, M., Minaguchi, T. and Yoshikawa, H. (2015). “High Pretreatment Plasma D-dimer Levels Are Associated With Poor Prognosis in Patients With Ovarian Cancer Independently of Venous Thromboembolism and Tumor Extension.” International Journal of Gynecological Cancer : Official Journal of the International Gynecological Cancer Society, 25(4), 593-598. https://doi.org/10.1097/IGC.0000000000000415.
14. Kawaguchi, R., Furukawa, N. and Kobayashi, H. (2012). “Cut-off Value of D-Dimer for Prediction of Deep Venous Thrombosis Before Treatment in Ovarian Cancer.” Journal of Gynecologic Oncology, 23(2), 98-102. https://doi.org/10.3802/jgo.2012.23.2.98
15. Liu, P., Wang, Y., Tong, L., Xu, Y., Zhang, W., Guo, Z. and Ni, H. (2015). “Elevated Preoperative Plasma D-Dimer Level is A Useful Predictor of Chemoresistance and Poor Disease Outcome for Serous Ovarian Cancer Patients.” Cancer Chemotherapy and Pharmacology, 76(6), 1163-1171. https://doi.org/10.1007/s00280-015-2900-y
16. Khorana, A. A. and Fine, R. L. (2004). “Pancreatic Cancer and Thromboembolic Disease.” The Lancet. Oncology, 5(11), 655–663. https://doi.org/10.1016/ S1470-2045(04)01606-7
17. Koldas, M., Gummus, M., Seker, M., Seval, H., Hulya, K., Dane, F., Kural, A., Gumus, A., Salepci, T. and Turhal, N. S. (2008). “Thrombin-Activatable Fibrinolysis Inhibitor Levels in Patients with Non-Small-Cell Lung Cancer.” Clinical Lung Cancer, 9(2), 112-115. https://doi.org/10.3816/clc.2008.n.017
18. Kawai, K. and Watanabe, T. (2014). “Colorectal Cancer And Hypercoagulability.” Surgery Today, 44(5), 797-803. https://doi.org/10.1007/s00595-013-0606-5
19. Tsimafeyeu, I. V, Demidov, L. V, Madzhuga, A. V, Somonova, O. V. and Yelizarova, A. L. (2009). “Hypercoagulability As A Prognostic Factor For Survival in Patients with Metastatic Renal Cell Carcinoma.” Journal of Experimental & Clinical Cancer Research : CR, 28, 30. https://doi.org/10.1186/1756-9966-28-30
20. Altiay, G., Ciftci, A., Demir, M., Kocak, Z., Sut, N., Tabakoglu, E., Hatipoglu, O. N. and Caglar, T. (2007). “High Plasma D-Dimer Level is Associated with Decreased Survival in Patients with Lung Cancer.” Clinical Oncology (Royal College of Radiologists (Great Britain)), 19(7), 494–498. https://doi.org/10.1016/j.clon. 2007.04.002
21. Dirix, L. Y., Salgado, R., Weytjens, R., Colpaert, C., Benoy, I., Huget, P., van Dam, P., Prové, A., Lemmens, J. and Vermeulen, P. (2002). “Plasma Fibrin D-Dimer Levels Correlate with Tumour Volume, Progression Rate and Survival in Patients With Metastatic Breast Cancer.” British Journal of Cancer, 86(3), 389-395. https://doi.org/10.1038/sj.bjc.6600069
22. Ay, C., Dunkler, D., Pirker, R., Thaler, J., Quehenberger, P., Wagner, O., Zielinski, C. and Pabinger, I. (2012). “High D-Dimer Levels Are Associated with Poor Prognosis in Cancer Patients.” Haematologica, 97(8), 1158–1164. https://doi.org/10.3324/haematol.2011.054718
23. Im, J. H., Fu, W., Wang, H., Bhatia, S. K., Hammer, D. A., Kowalska, M. A. and Muschel, R. J. (2004). “Coagulation Facilitates Tumor Cell Spreading in the Pulmonary Vasculature during Early Metastatic Colony Formation.” Cancer Research, 64(23), 8613-8619. https://doi.org/10.1158/0008-5472.CAN-04-2078
24. Caine, G. J., Stonelake, P. S., Lip, G. Y. H. and Kehoe, S. T. (n.d.). “The Hypercoagulable State of Malignancy: Pathogenesis and Current Debate.” Neoplasia (New York, N.Y.), 4(6), 465-473. https://doi.org/10.1038/sj.neo. 7900263
25. Bluff, J. E., Brown, N. J., Reed, M. W. R. and Staton, C. A. (2008). “Tissue Factor, Angiogenesis and Tumour Progression.” Breast Cancer Research : BCR, 10(2), 204. https://doi.org/10.1186/bcr1871
26. Dirix, L. Y., Salgado, R., Weytjens, R., Colpaert, C., Benoy, I., Huget, P., van Dam, P., Prové, A., Lemmens, J. and Vermeulen, P. (2002). “Plasma Fibrin D-Dimer Levels Correlate with Tumour Volume, Progression Rate and Survival in Patients With Metastatic Breast Cancer.” British Journal of Cancer, 86(3), 389-395. https://doi.org/10.1038/sj.bjc.6600069
27. Wu, J., Fu, Z., Liu, G., Xu, P., Xu, J. and Jia, X. (2017). “Clinical Significance of Plasma D-Dimer in Ovarian Cancer: A Meta-Analysis.” Medicine, 96(25), e7062. https://doi.org/10.1097/MD.0000000000007062

Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi

Yıl 2022, Cilt: 11 Sayı: 1, 153 - 157, 19.03.2022

Nazlı Topfedaisi Özkan Nezaket Kadıoğlu Burcu Timur Mehmet Mutlu Meydanlı

https://doi.org/10.37989/gumussagbil.1049371

Öz

Over kanseri jinekolojik kanserler arasında kansere bağlı ölümlerin önde gelen nedenidir. Kanser hastalarında özellikle ileri evrede, venöz tromboembolizm yokken bile hemostatik aktivasyona bağlı hiperkoagülasyon ve artmış fibrinoliz sıklıkla gözlenir. Bu çalışma ile yüksek dereceli seröz karsinom olgularında operasyon öncesi ölçülen plazma d-dimer düzeyinin klinik önemi ve prognostik değerini incelemeyi amaçladık. Retrosptektif olarak yapılan çalışmamızda Dr. Zekai Tahir Burak Eğitim ve Araştırma Hastanesi Jinekolojik Onkoloji Kliniği’nde 2013-2017 tarihleri arasında primer yüksek dereceli seröz over kanseri (HGSK) tanısı alan ve operasyondan önceki 15 gün içinde D-dimer testi yapılan 142 hasta dahil edildi. Tanı anındaki yaş, tedavi öncesi plazma D-dimer düzeyi, asit varlığı, rezidüel tümör, CA125 seviyesi, FIGO evresi ve demografik bilgileri karşılaştırıldı. Ortalama yaşları 55.25 ±10.84 olan hastaların 52’ sinde (%36,6) normal, 90’ ında(%63,4) D-dimer seviyeleri yüksek olarak saptandı. D-dimer düzeyi yüksek olan ve olmayan olgularda 60 yaş sınır alındığında anlamlı farklılık saptanmazken, D-dimer düzeyi yüksek olan olgularda FIGO evresi (III-IV) daha yüksek olup (p<0,001) masif asit varlığı (p<0,001) ve rezidü tümör görülme olasılığı daha yüksek bulundu (p<0,001). Tümör yükü ve anjiyogenez ile ilgili sitokinler olan interlökin 6, serum vasküler endotelyal büyüme faktörü (SVEGF) ve platelet vaskuler endotelyal büyüme faktörü (PDEGF) ile plazma D-dimer seviyesi arasında pozitif korelasyonun varlığını gösteren çalışmalar; pıhtılaşma aktivasyonu ve fibrinoliz ile tümör anjiyogenezi, invazyon, progresyon ve metastatik yayılım arasında bir korelasyonun varlığını göstermektedir. Çalışmamızın sonuçlarına göre HGSK hastalarında yüksek plazma D-dimer düzeyleri ileri evre hastalık ve yüksek rezidü hastalık yükü ile ilişkili gözükmektedir. Kolay ölçülebilir bir parametre olması nedeni ile klinik uygulamada kullanılabilir bir belirteç olduğunu düşündürmektedir.

Anahtar Kelimeler

Yüksek dereceli seröz over kanseri, hiperkoagülasyon, fibrinolizis, D-dimer düzeyi

Kaynakça

1. Ferlay, J., Soerjomataram, I., Dikshit, R., Eser, S., Mathers, C., Rebelo, M., Parkin, D. M., Forman, D. and Bray, F. (2015). “Cancer Incidence and Mortality Worldwide: Sources, Methods and Major Patterns in GLOBOCAN 2012.” International Journal of Cancer, 136(5), E359-86. https://doi.org/10.1002/ijc.29210
2. Kurman, R. J. and Shih, I.-M. (2016). “The Dualistic Model of Ovarian Carcinogenesis: Revisited, Revised, and Expanded.” The American Journal of Pathology, 186(4), 733–747. https://doi.org/10.1016/j.ajpath.2015. 11.011
3. Koshiyama, M., Matsumura, N. and Konishi, I. (2017). “Subtypes of Ovarian Cancer and Ovarian Cancer Screening.” Diagnostics (Basel, Switzerland), 7(1), 1-5. https://doi.org/10.3390/diagnostics7010012
4. Cooke, S. L., & Brenton, J. D. (2011). “Evolution of platinum resistance in high-grade serous ovarian cancer”. The Lancet. Oncology, 12(12), 1169–1174. https://doi.org/10.1016/S1470-2045(11)70123-1
5. Ogata, Y., Heppelmann, C. J., Heppelmann, C. J., Charlesworth, M. C., Madden, B. J., Miller, M. N., Kalli, K. R., Cliby, W. A., Bergen, H. R., Saggese, D. A. and Muddiman, D. C. (2006). “Elevated Levels of Phosphorylated Fibrinogen-Alpha-Isoforms and Differential Expression of Other Post-Translationally Modified Proteins in The Plasma of Ovarian Cancer Patients.” Journal of Proteome Research, 5(12), 3318-3325. https://doi.org/10.1021/pr060344+
6. Ogata, Y., Heppelmann, C. J., Heppelmann, C. J., Charlesworth, M. C., Madden, B. J., Miller, M. N., Kalli, K. R., Cliby, W. A., Bergen, H. R., Saggese, D. A. and Muddiman, D. C. (2006). “Elevated Levels of Phosphorylated Fibrinogen-Alpha-Isoforms and Differential Expression of Other Post-Translationally Modified Proteins in The Plasma of Ovarian Cancer Patients.” Journal of Proteome Research, 5(12), 3318-3325. https://doi.org/10.1021/pr060344+
7. Miralles, C., Orea, M., España, P., Provencio, M., Sánchez, A., Cantos, B., Cubedo, R., Carcereny, E., Bonilla, F. and Gea, T. (2003). “Cancer Antigen 125 Associated with Multiple Benign and Malignant Pathologies.” Annals of Surgical Oncology, 10(2), 150–154. https://doi.org/10.1245/aso.2003.05.015
8. Sakurai, M., Matsumoto, K., Gosho, M., Sakata, A., Hosokawa, Y., Tenjimbayashi, Y., Katoh, T., Shikama, A., Komiya, H., Michikami, H., Tasaka, N., Akiyama-Abe, A., Nakao, S., Ochi, H., Onuki, M., Minaguchi, T., Yoshikawa, H. and Satoh, T. (2017). “Expression of Tissue Factor in Epithelial Ovarian Carcinoma Is Involved in the Development of Venous Thromboembolism.” International Journal of Gynecological Cancer : Official Journal of the International Gynecological Cancer Society, 27(1), 37-43. https://doi.org/10.1097/IGC.0000000000000848
9. Varol A, Köktürk N, Kılıç H, Aydoğdu M, Ekim NN. (2012). “The Role of Quantitative D-Dimer Levels in The Follow-Up and Differential Diagnosis of Pulmonary Thromboembolism and Community- Acquired Pneumonia.” Turk J Med Sci, 42, 639-47.
10. Lin, Y., Liu, Z., Qiu, Y., Zhang, J., Wu, H., Liang, R., Chen, G., Qin, G., Li, Y. and Zou, D. (2018). “Clinical Significance of Plasma D-Dimer And Fibrinogen in Digestive Cancer: A Systematic Review and Meta-Analysis.” European Journal of Surgical Oncology : The Journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology, 44(10), 1494-1503. https://doi.org/10.1016/j.ejso.2018.07.052
11. Zhu, L, Liu, B., Zhao, Y., Liu, L., Yang, C., Yang, Y. and Zhong, H. (2014). “High Levels of D-Dimer Correlated with Disease Status and Poor Prognosis of Inoperable Metastatic Colorectal Cancer Patients Treated with Bevacizumab.” J Cancer Res Ther, 10, 246-51.
12. Chen, L., Wang, X., Shu, J., Xu, S., Wu, Q. and Yu, Y. (2019). “Diagnostic Value of Serum D-Dimer, CA125, and Neutrophil-To-Lymphocyte Ratio in Differentiating Ovarian Cancer and Endometriosis.” International Journal of Gynaecology and Obstetrics: The Official Organ of the International Federation of Gynaecology and Obstetrics, 147(2), 212–218. https://doi.org/10.1002/ijgo.12949
13. Sakurai, M., Satoh, T., Matsumoto, K., Michikami, H., Nakamura, Y., Nakao, S., Ochi, H., Onuki, M., Minaguchi, T. and Yoshikawa, H. (2015). “High Pretreatment Plasma D-dimer Levels Are Associated With Poor Prognosis in Patients With Ovarian Cancer Independently of Venous Thromboembolism and Tumor Extension.” International Journal of Gynecological Cancer : Official Journal of the International Gynecological Cancer Society, 25(4), 593-598. https://doi.org/10.1097/IGC.0000000000000415.
14. Kawaguchi, R., Furukawa, N. and Kobayashi, H. (2012). “Cut-off Value of D-Dimer for Prediction of Deep Venous Thrombosis Before Treatment in Ovarian Cancer.” Journal of Gynecologic Oncology, 23(2), 98-102. https://doi.org/10.3802/jgo.2012.23.2.98
15. Liu, P., Wang, Y., Tong, L., Xu, Y., Zhang, W., Guo, Z. and Ni, H. (2015). “Elevated Preoperative Plasma D-Dimer Level is A Useful Predictor of Chemoresistance and Poor Disease Outcome for Serous Ovarian Cancer Patients.” Cancer Chemotherapy and Pharmacology, 76(6), 1163-1171. https://doi.org/10.1007/s00280-015-2900-y
16. Khorana, A. A. and Fine, R. L. (2004). “Pancreatic Cancer and Thromboembolic Disease.” The Lancet. Oncology, 5(11), 655–663. https://doi.org/10.1016/ S1470-2045(04)01606-7
17. Koldas, M., Gummus, M., Seker, M., Seval, H., Hulya, K., Dane, F., Kural, A., Gumus, A., Salepci, T. and Turhal, N. S. (2008). “Thrombin-Activatable Fibrinolysis Inhibitor Levels in Patients with Non-Small-Cell Lung Cancer.” Clinical Lung Cancer, 9(2), 112-115. https://doi.org/10.3816/clc.2008.n.017
18. Kawai, K. and Watanabe, T. (2014). “Colorectal Cancer And Hypercoagulability.” Surgery Today, 44(5), 797-803. https://doi.org/10.1007/s00595-013-0606-5
19. Tsimafeyeu, I. V, Demidov, L. V, Madzhuga, A. V, Somonova, O. V. and Yelizarova, A. L. (2009). “Hypercoagulability As A Prognostic Factor For Survival in Patients with Metastatic Renal Cell Carcinoma.” Journal of Experimental & Clinical Cancer Research : CR, 28, 30. https://doi.org/10.1186/1756-9966-28-30
20. Altiay, G., Ciftci, A., Demir, M., Kocak, Z., Sut, N., Tabakoglu, E., Hatipoglu, O. N. and Caglar, T. (2007). “High Plasma D-Dimer Level is Associated with Decreased Survival in Patients with Lung Cancer.” Clinical Oncology (Royal College of Radiologists (Great Britain)), 19(7), 494–498. https://doi.org/10.1016/j.clon. 2007.04.002
21. Dirix, L. Y., Salgado, R., Weytjens, R., Colpaert, C., Benoy, I., Huget, P., van Dam, P., Prové, A., Lemmens, J. and Vermeulen, P. (2002). “Plasma Fibrin D-Dimer Levels Correlate with Tumour Volume, Progression Rate and Survival in Patients With Metastatic Breast Cancer.” British Journal of Cancer, 86(3), 389-395. https://doi.org/10.1038/sj.bjc.6600069
22. Ay, C., Dunkler, D., Pirker, R., Thaler, J., Quehenberger, P., Wagner, O., Zielinski, C. and Pabinger, I. (2012). “High D-Dimer Levels Are Associated with Poor Prognosis in Cancer Patients.” Haematologica, 97(8), 1158–1164. https://doi.org/10.3324/haematol.2011.054718
23. Im, J. H., Fu, W., Wang, H., Bhatia, S. K., Hammer, D. A., Kowalska, M. A. and Muschel, R. J. (2004). “Coagulation Facilitates Tumor Cell Spreading in the Pulmonary Vasculature during Early Metastatic Colony Formation.” Cancer Research, 64(23), 8613-8619. https://doi.org/10.1158/0008-5472.CAN-04-2078
24. Caine, G. J., Stonelake, P. S., Lip, G. Y. H. and Kehoe, S. T. (n.d.). “The Hypercoagulable State of Malignancy: Pathogenesis and Current Debate.” Neoplasia (New York, N.Y.), 4(6), 465-473. https://doi.org/10.1038/sj.neo. 7900263
25. Bluff, J. E., Brown, N. J., Reed, M. W. R. and Staton, C. A. (2008). “Tissue Factor, Angiogenesis and Tumour Progression.” Breast Cancer Research : BCR, 10(2), 204. https://doi.org/10.1186/bcr1871
26. Dirix, L. Y., Salgado, R., Weytjens, R., Colpaert, C., Benoy, I., Huget, P., van Dam, P., Prové, A., Lemmens, J. and Vermeulen, P. (2002). “Plasma Fibrin D-Dimer Levels Correlate with Tumour Volume, Progression Rate and Survival in Patients With Metastatic Breast Cancer.” British Journal of Cancer, 86(3), 389-395. https://doi.org/10.1038/sj.bjc.6600069
27. Wu, J., Fu, Z., Liu, G., Xu, P., Xu, J. and Jia, X. (2017). “Clinical Significance of Plasma D-Dimer in Ovarian Cancer: A Meta-Analysis.” Medicine, 96(25), e7062. https://doi.org/10.1097/MD.0000000000007062

Toplam 27 adet kaynakça vardır.

Ayrıntılar

Birincil Dil	Türkçe
Konular	Sağlık Kurumları Yönetimi
Bölüm	Araştırma Makaleleri
Yazarlar	Nazlı Topfedaisi Özkan 0000-0001-9399-0637 Nezaket Kadıoğlu 0000-0002-5285-9277 Burcu Timur 0000-0001-8769-5949 Mehmet Mutlu Meydanlı 0000-0001-6763-9720
Yayımlanma Tarihi	19 Mart 2022
Yayımlandığı Sayı	Yıl 2022 Cilt: 11 Sayı: 1

Kaynak Göster

APA	Topfedaisi Özkan, N., Kadıoğlu, N., Timur, B., Meydanlı, M. M. (2022). Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi, 11(1), 153-157. https://doi.org/10.37989/gumussagbil.1049371
AMA	Topfedaisi Özkan N, Kadıoğlu N, Timur B, Meydanlı MM. Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi. Mart 2022;11(1):153-157. doi:10.37989/gumussagbil.1049371
Chicago	Topfedaisi Özkan, Nazlı, Nezaket Kadıoğlu, Burcu Timur, ve Mehmet Mutlu Meydanlı. “Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi”. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi 11, sy. 1 (Mart 2022): 153-57. https://doi.org/10.37989/gumussagbil.1049371.
EndNote	Topfedaisi Özkan N, Kadıoğlu N, Timur B, Meydanlı MM (01 Mart 2022) Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi 11 1 153–157.
IEEE	N. Topfedaisi Özkan, N. Kadıoğlu, B. Timur, ve M. M. Meydanlı, “Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi”, Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi, c. 11, sy. 1, ss. 153–157, 2022, doi: 10.37989/gumussagbil.1049371.
ISNAD	Topfedaisi Özkan, Nazlı vd. “Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi”. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi 11/1 (Mart 2022), 153-157. https://doi.org/10.37989/gumussagbil.1049371.
JAMA	Topfedaisi Özkan N, Kadıoğlu N, Timur B, Meydanlı MM. Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi. 2022;11:153–157.
MLA	Topfedaisi Özkan, Nazlı vd. “Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi”. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi, c. 11, sy. 1, 2022, ss. 153-7, doi:10.37989/gumussagbil.1049371.
Vancouver	Topfedaisi Özkan N, Kadıoğlu N, Timur B, Meydanlı MM. Plazma D-Dimer Düzeyinin Yüksek Dereceli Seröz Over Kanseri Olan Olgularda Prognostik Verilerle Olan İlişkisi. Gümüşhane Üniversitesi Sağlık Bilimleri Dergisi. 2022;11(1):153-7.

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