Article Data

  • Views 2072
  • Dowloads 135

Original Research

Open Access

Poor prognosis associated with venous thromboembolism in Asian patients with ovarian clear cell carcinoma

  • Ka Yu Tse1,*,
  • Philip Pun Ching Ip2
  • Suk Kwan Lau1
  • Tong Yow Ng1
  • Kar Fai Tam1
  • Annie Nga Yin Cheung2
  • Hextan Yuen Sheung Ngan1

1Department of Obstetrics and Gynaecology, Queen Mary Hospital, the University of Hong Kong, Hong Kong, China

2Department of Pathology, Queen Mary Hospital, the University of Hong Kong, Hong Kong, China

DOI: 10.12892/ejgo3972.2018 Vol.39,Issue 6,December 2018 pp.903-910

Published: 15 December 2018

*Corresponding Author(s): Ka Yu Tse E-mail: seky@hku.hk

PDF (1.03 MB) View Full-text

Abstract

Purpose of Investigation: To evaluate the incidence and prognostic implications of venous thromboembolism (VTE) in Asian patients with ovarian clear cell carcinoma (CCC). Materials and Methods: Between July 1987 and December 2005, 144 CCC patients were identified. The clinical outcomes of those with (case) and without (control) VTE were analyzed retrospectively. Results: After a mean follow-up of 131.2 ± 52.2 months, 11.1% (16/144) developed VTE and only one occurred in the perioperative period. Compared to the control, the case group was less responsive to chemotherapy (57.1% vs. 85.1%, p = 0.01) with shorter duration of response to chemotherapy (4.7 months vs. 83.6 months; p < 0.001), higher recurrence / progressive disease rate (100.0% vs. 37.2%, p < 0.001), shorter median disease-free survival (DFS) (0 months vs. 70.8 months; p < 0.001), and overall survival (OS) (16.5 months vs. 88.0 months; p < 0.001). The median interval from the diagnosis of VTE to death was 43.0 (range 1–394) days, and the 60-day mortality rate was 56.3%. Multivariate analysis showed that duration of chemotherapy response for more than one year was independently correlated with the DFS, while VTE, stage, and the chemotherapy response duration were independent prognosticators for OS. Conclusion: VTE is rare in Asian patients with CCC and care is needed when giving it to these patients in view of possible haemorrhagic complications. When VTE occurs, it is associated with high mortality.

Keywords

Ovarian carcinoma; Clear cell; Venous thromboembolism.

Cite and Share

Ka Yu Tse, Philip Pun Ching Ip, Suk Kwan Lau, Tong Yow Ng, Kar Fai Tam, Annie Nga Yin Cheung, Hextan Yuen Sheung Ngan. Poor prognosis associated with venous thromboembolism in Asian patients with ovarian clear cell carcinoma. European Journal of Gynaecological Oncology. 2018; 39(6): 903-910. doi: 10.12892/ejgo3972.2018

References

[1] Trousseau A.: “Phlegmasia alba dolens. Clinique Medicale del’Hotel- Dieu de Paris, 3”. London: New Sydenham Society, 1865.

[2] Uno K., Homma S., Satoh T., Nakanishi K., Abe D., Matsumoto K., et al.: “Tissue factor expression as a possible determinant of thromboembolism in ovarian cancer”. Br. J. Cancer, 2007, 96, 290.

[3] Abu Saadeh F., Norris L., O’Toole S., Mohamed B.M., Langhe R., O’Leary J., et al.: “Tumour expresion of tissue factor and tissue factor pathway inhibitor in ovarian cancer- relationship with venous thrombosis risk”. Thromb. Res., 2013, 132, 627.

[4] Wang X., Wang E., Kavanagh J.J., Freedman R.S.: “Ovarian cancer, the coagulation pathway, and inflammation”. J. Transl. Med., 2005, 3, 25.

[5] Fernandez P.M., Rickles FR: “Tumor angiogenesis and blood coagulation”. In: Lugassy G.F.A., Kakkar A.K., Rickles F.R., (eds). Thrombosis and Cancer. London, United Kingdom: Martin Dunitz, 2004, 69.

[6] Tateo S., Mereu L., Salamano S., Klersy C., Barone M., Spyropoulos A.C., et al.: “Ovarian cancer and venous thromboembolic risk”. Gynecol. Oncol., 2005, 99, 119.

[7] Rodriguez A.O., Wun T., Chew H., Zhou H., Harvey D., White R.H.: “Venous thromboembolism in ovarian cancer”. Gynecol. Oncol., 2007, 105, 784.

[8] Saadeh F.A., Norris L., O’Toole S., Gleeson N.: “Venous thromboembolism in ovarian cancer: incidence, risk factors and impact on survival”. Eur. J. Obstet. Gynecol. Reprod. Biol., 2013, 170, 214.

[9] Matsuura Y., Robertson G., Marsden D.E., Kim S.N., Gebski V., Hacker N.F.: “Thromboembolic complications in patients with clear cell carcinoma of the ovary”. Gynecol. Oncol., 2007, 104, 406.

[10] Anglesio M.S., Carey M.S., Kobel M., Mackay H., Huntsman D.G., Vancouver Ovarian Clear Cell Symposium S.: “Clear cell carcinoma of the ovary: a report from the first Ovarian Clear Cell Symposium, June 24th, 2010”. Gynecol. Oncol., 2011, 121, 407.

[11] Sugiyama T., Kamura T., Kigawa J., Terakawa N., Kikuchi Y., Kita T., et al.: “Clinical characteristics of clear cell carcinoma of the ovary: a distinct histologic type with poor prognosis and resistance to platinum-based chemotherapy”. Cancer, 2000, 88, 2584.

[12] Itamochi H., Kigawa J., Terakawa N.: “Mechanisms of chemoresistance and poor prognosis in ovarian clear cell carcinoma”. Cancer Sci., 2008, 99, 653.

[13] Recio F.O., Piver M.S., Hempling R.E., Driscoll D.L.: “Lack of improved survival plus increase in thromboembolic complications in patients with clear cell carcinoma of the ovary treated with platinum versus nonplatinum-based chemotherapy”. Cancer, 1996, 78, 2157.

[14] Goff B.A., Sainz de la Cuesta R., Muntz H.G., Fleischhacker D., Ek M., Rice L.W., et al.: “Clear cell carcinoma of the ovary: a distinct histologic type with poor prognosis and resistance to platinum-based chemotherapy in stage III disease”. Gynecol. Oncol., 1996, 60, 412.

[15] Pather S., Quinn M.A.: “Clear-cell cancer of the ovary-is it chemosensitive?” Int. J. Gynecol. Cancer, 2005, 15, 432.

[16] Duska L.R., Garrett L., Henretta M., Ferriss J.S., Lee L., Horowitz N.: “When ‘never-events’ occur despite adherence to clinical guidelines: the case of venous thromboembolism in clear cell cancer of the ovary compared with other epithelial histologic subtypes”. Gynecol. Oncol., 2010, 116, 374.

[17] Diaz E.S., Walts A.E., Karlan B.Y., Walsh C.S.: “Venous thromboembolism during primary treatment of ovarian clear cell carcinoma is associated with decreased survival”. Gynecol. Oncol., 2013, 131, 541.

[18] Lyman G.H., Khorana A.A., Kuderer N.M., Lee A.Y., Arcelus J.I., Balaban E.P., et al.: “Venous thromboembolism prophylaxis and treatment in patients with cancer: American Society of Clinical Oncology clinical practice guideline update”. J. Clin. Oncol., 2013, 31, 2189.

[19] Gould M.K., Garcia D.A., Wren S.M., Karanicolas P.J., Arcelus J.I., Heit J.A., et al.: “Prevention of VTE in nonorthopedic surgical patients: Antithrombotic Therapy and Prevention of Thrombosis, 9th ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines”. Chest, 2012, 141, e227S.

[20] National Collaborating Centre for Acute and Chronic Conditions: “Venous thromboembolism: reducing the risk: reducing the risk of venous thromboembolism (deep vein thrombosis and pulmonary embolism) in patients admitted to hospital. NICE clinical guideline”. London: National Institute for Health and Clinical Excellence, 2010, 1.

[21] Teoh D., Berchuck A., Alvarez Secord A., Lee P.S., Lowery W.J., Sfakianos G.P., et al.: “Cost comparison of strategies for the management of venous thromboembolic event risk following laparotomy for ovarian cancer”. Gynecol. Oncol., 2011, 122, 467.

[22] Uppal S., Hernandez E., Dutta M., Dandolu V., Rose S., Hartenbach E.: “Prolonged postoperative venous thrombo-embolism prophylaxis is cost-effective in advanced ovarian cancer patients”. Gynecol. Oncol., 2012, 127, 631.

[23] Weida D., Patrick L.Y., Andrew Y.W.: “Is it safe to perform operation for colorectal malignancy in Chinese patients without DVT prophylaxis? An 8-year experience from a regional hospital in Hong Kong”. Chin. Med. J. (Engl.), 2010, 123, 1973.

[24] Cheuk B.L., Cheung G.C., Cheng S.W.: “Epidemiology of venous thromboembolism in a Chinese population”. Br. J. Surg., 2004, 91, 424.

[25] Magazzino F., Katsaros D., Ottaiano A., Gadducci A., Pisano C., Sorio R., et al.: “Surgical and medical treatment of clear cell ovarian cancer: results from the multicenter Italian Trials in Ovarian Cancer (MITO) 9 retrospective study”. Int. J. Gynecol. Cancer, 2011, 21, 1063.

[26] Mahdi H., Moslemi-Kebria M., Levinson K.L., Gojayev A., Lockhart D., Ali-Fehmi R., et al.: “Prevalence and prognostic impact of lymphadenectomy and lymph node metastasis in clinically earlystage ovarian clear cell carcinoma”. Int. J. Gynecol Cancer, 2013, 23, 1226.

[27] Suzuki S., Kajiyama H., Shibata K., Ino K., Nawa A., Sakakibara K., et al.: “Is there any association between retroperitoneal lymphadenectomy and survival benefit in ovarian clear cell carcinoma patients?” Ann. Oncol., 2008, 19, 1284.

[28] Sorensen H.T., Mellemkjaer L., Olsen J.H., Baron J.A.: “Prognosis of cancers associated with venous thromboembolism”. N. Engl. J. Med., 2000, 343, 1846.

[29] Chew H.K., Wun T., Harvey D., Zhou H., White R.H.: “Incidence of venous thromboembolism and its effect on survival among patients with common cancers”. Arch. Intern. Med., 2006, 166, 458.

[30] Black D., Iasonos A., Ahmed H., Chi D.S., Barakat R.R., Abu-Rustum N.R.: “Effect of perioperative venous thromboembolism on survival in ovarian, primary peritoneal, and fallopian tube cancer”. Gynecol. Oncol., 2007, 107, 66.

[31] Fotopoulou C., duBois A., Karavas A.N., Trappe R., Aminossadati B., Schmalfeldt B., et al.: “Incidence of venous thromboembolism in patients with ovarian cancer undergoing platinum/paclitaxel-containing first-line chemotherapy: an exploratory analysis by the Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group”. J. Clin. Oncol., 2008, 26, 2683.

[32] Rak J., Yu J.L., Luyendyk J., Mackman N.: “Oncogenes, trousseau syndrome, and cancer-related changes in the coagulome of mice and humans”. Cancer Res., 2006, 66, 10643.

[33] Liu Y., Jiang P., Capkova K., Xue D., Ye L., Sinha S.C., et al.: “Tissue factor-activated coagulation cascade in the tumor microenvironment is critical for tumor progression and an effective target for therapy”. Cancer Res., 2011, 71, 6492.

[34] Kasthuri R.S., Taubman M.B., Mackman N.: “Role of tissue factor in cancer”. J. Clin. Oncol., 2009, 27, 4834.

[35] Han L.Y., Landen C.N., Jr., Kamat A.A., Lopez A., Bender D.P., Mueller P., et al.: “Preoperative serum tissue factor levels are an independent prognostic factor in patients with ovarian carcinoma”. J. Clin. Oncol., 2006, 24, 755.

[36] Kakkar A.K., Levine M.N., Kadziola Z., Lemoine N.R., Low V., Patel H.K., et al.: “Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: the fragmin advanced malignancy outcome study (FAMOUS)”. J. Clin. Oncol., 2004, 22, 1944.

[37] Klerk C.P., Smorenburg S.M., Otten H.M., Lensing A.W., Prins M.H., Piovella F., et al.: “The effect of low molecular weight heparin on survival in patients with advanced malignancy”. J. Clin. Oncol., 2005, 23, 2130.

[38] Akl E.A., Gunukula S., Barba M., Yosuico V.E., van Doormaal F.F., Kuipers S., et al.: “Parenteral anticoagulation in patients with cancer who have no therapeutic or prophylactic indication for anticoagulation”. Cochrane Database Syst. Rev., 2011, CD006652.

[39] Che D.H., Cao J.Y., Shang L.H., Man Y.C., Yu Y.: “The efficacy and safety of low-molecular-weight heparin use for cancer treatment: a meta-analysis”. Eur. J. Intern. Med., 2013, 24, 433.

[40] Elit L.M., Lee A.Y., Parpia S., Swystun L.L., Liaw P.C., Hoskins P., et al.: “Dalteparin low molecular weight heparin (LMWH) in ovarian cancer: a phase II randomized study”. Thromb. Res., 2012, 130, 894.

Submission Turnaround Time

Top