Skip to main content
Top
Published in: Archives of Gynecology and Obstetrics 5/2020

01-05-2020 | Ovarian Cancer | Gynecologic Oncology

Significance of lymph node ratio on survival of women with borderline ovarian tumors

Authors: David J. Nusbaum, Rachel S. Mandelbaum, Hiroko Machida, Shinya Matsuzaki, Lynda D. Roman, Anil K. Sood, David M. Gershenson, Koji Matsuo

Published in: Archives of Gynecology and Obstetrics | Issue 5/2020

Login to get access

Abstract

Purpose

To assess the qualitative and quantitative measures of the effect of pelvic lymph node involvement on survival of women with borderline ovarian tumors (BOTs).

Methods

This is a retrospective study examining the Surveillance, Epidemiology, and End Results Program between 1988 and 2003. Women with stage T1-3 BOTs who had results of pelvic lymph node status at surgery were included. The effect of lymph node involvement on cause-specific survival (CSS) was evaluated using multivariable analysis with the following approaches: (1) any involvement, (2) involvement of multiple nodes (≥ 2 nodes), and (3) lymph node ratio (LNR), defined as the ratio of the number of tumor-containing lymph nodes to the total number of harvested lymph nodes.

Results

A total of 1524 women were examined for analysis. Median count of sampled nodes was 8 (interquartile range 3–15), and there were 81 (5.3%, 95% confidence interval [CI] 4.2–6.4) women who had lymph node involvement. Median follow-up was 15.8 (interquartile range 13.8–18.9) years, and 83 (5.4%) women died of BOTs. After controlling for age, histology, stage, and tumor size, only LNR remained an independent prognostic factor for decreased CSS (adjusted hazard ratio [HR] per percentage unit 1.015, 95% CI 1.003–1.026, P = 0.014), whereas any involvement (adjusted HR 1.700, 95% CI 0.843–3.430, P = 0.138) and involvement of multiple nodes (adjusted HR 1.644, 95% CI 0.707–3.823, P = 0.249) did not. On cutoff analysis, LNR ≥ 13% had the largest magnitude of significance on multivariable analysis of CSS (adjusted HR 2.399, 95% CI 1.163–4.947, P = 0.018).

Conclusion

Our study suggests that high pelvic LNR may be a prognostic factor associated with decreased CSS in women with BOTs.
Literature
1.
go back to reference Matsuo K, Sood AK, Gershenson DM (2015) Management of early-stage ovarian cancer. In: Bristow RE, Karlan BY (eds) Surgery for ovarian cancer: Principles and practice, Chapt 3, 3rd edn, vol 3. Informa Healthcare, New York, pp 67–104 Matsuo K, Sood AK, Gershenson DM (2015) Management of early-stage ovarian cancer. In: Bristow RE, Karlan BY (eds) Surgery for ovarian cancer: Principles and practice, Chapt 3, 3rd edn, vol 3. Informa Healthcare, New York, pp 67–104
2.
go back to reference Sherman ME, Mink PJ, Curtis R, Cote TR, Brooks S, Hartge P, Devesa S (2004) Survival among women with borderline ovarian tumors and ovarian carcinoma: a population-based analysis. Cancer 100:1045–1052PubMed Sherman ME, Mink PJ, Curtis R, Cote TR, Brooks S, Hartge P, Devesa S (2004) Survival among women with borderline ovarian tumors and ovarian carcinoma: a population-based analysis. Cancer 100:1045–1052PubMed
3.
go back to reference Kanat-Pektas M, Ozat M, Gungor T, Sahin I, Yalcin H, Ozdal B (2011) Complete lymph node dissection: is it essential for the treatment of borderline epithelial ovarian tumors? Arch Gynecol Obstet 283:879–884PubMed Kanat-Pektas M, Ozat M, Gungor T, Sahin I, Yalcin H, Ozdal B (2011) Complete lymph node dissection: is it essential for the treatment of borderline epithelial ovarian tumors? Arch Gynecol Obstet 283:879–884PubMed
4.
go back to reference Pirimoglu ZM, Afsin Y, Guzelmeric K, Yilmaz M, Unal O, Turan MC (2008) Is it necessary to do retroperitoneal evaluation in borderline epithelial ovarian tumors? Arch Gynecol Obstet 277:411–414PubMed Pirimoglu ZM, Afsin Y, Guzelmeric K, Yilmaz M, Unal O, Turan MC (2008) Is it necessary to do retroperitoneal evaluation in borderline epithelial ovarian tumors? Arch Gynecol Obstet 277:411–414PubMed
5.
go back to reference Morice P, Camatte S, Rey A, Atallah D, Lhomme C, Pautier P, Pomel C, Coté J-F, Haie-Meder C, Duvillard P (2003) Prognostic factors for patients with advanced stage serous borderline tumours of the ovary. Ann Oncol 14:592–598PubMed Morice P, Camatte S, Rey A, Atallah D, Lhomme C, Pautier P, Pomel C, Coté J-F, Haie-Meder C, Duvillard P (2003) Prognostic factors for patients with advanced stage serous borderline tumours of the ovary. Ann Oncol 14:592–598PubMed
6.
go back to reference Guvenal T, Dursun P, Hasdemir PS, Hanhan M, Guven S, Yetimalar H, Goksedef BP, Sakarya DK, Doruk A, Terek MC, Saatli B, Guzin K, Corakci A, Deger E, Celik H, Cetin A, Ozsaran A, Ozbakkaloglu A, Kolusari A, Celik C, Keles R, Sagir FG, Dilek S, Uslu T, Dikmen Y, Altundag O, Ayhan A (2013) Effect of surgical staging on 539 patients with borderline ovarian tumors: a Turkish Gynecologic Oncology Group study. Gynecol Oncol 131:546–550PubMed Guvenal T, Dursun P, Hasdemir PS, Hanhan M, Guven S, Yetimalar H, Goksedef BP, Sakarya DK, Doruk A, Terek MC, Saatli B, Guzin K, Corakci A, Deger E, Celik H, Cetin A, Ozsaran A, Ozbakkaloglu A, Kolusari A, Celik C, Keles R, Sagir FG, Dilek S, Uslu T, Dikmen Y, Altundag O, Ayhan A (2013) Effect of surgical staging on 539 patients with borderline ovarian tumors: a Turkish Gynecologic Oncology Group study. Gynecol Oncol 131:546–550PubMed
7.
go back to reference Winter WE III, Kucera PR, Rodgers W, McBroom JW, Olsen C, Maxwell GL (2002) Surgical staging in patients with ovarian tumors of low malignant potential. Obstet Gynecol 100:671–676PubMed Winter WE III, Kucera PR, Rodgers W, McBroom JW, Olsen C, Maxwell GL (2002) Surgical staging in patients with ovarian tumors of low malignant potential. Obstet Gynecol 100:671–676PubMed
8.
go back to reference Lesieur B, Kane A, Duvillard P, Gouy S, Pautier P, Lhomme C, Morice P, Uzan C (2011) Prognostic value of lymph node involvement in ovarian serous borderline tumors. Am J Obstet Gynecol 204(438):e1–e7 Lesieur B, Kane A, Duvillard P, Gouy S, Pautier P, Lhomme C, Morice P, Uzan C (2011) Prognostic value of lymph node involvement in ovarian serous borderline tumors. Am J Obstet Gynecol 204(438):e1–e7
9.
go back to reference Qian XQ, Hua XP, Wu JH, Shen YM, Cheng XD, Wan XY (2018) Clinical predictors of recurrence and prognostic value of lymph node involvement in the serous borderline ovarian tumor. Int J Gynecol Cancer 28:279–284PubMed Qian XQ, Hua XP, Wu JH, Shen YM, Cheng XD, Wan XY (2018) Clinical predictors of recurrence and prognostic value of lymph node involvement in the serous borderline ovarian tumor. Int J Gynecol Cancer 28:279–284PubMed
10.
go back to reference Cho Y-H, Kim D-Y, Kim J-H, Kim Y-M, Kim K-R, Kim Y-T, Nam J-H (2006) Is complete surgical staging necessary in patients with stage I mucinous epithelial ovarian tumors? Gynecol Oncol 103:878–882PubMed Cho Y-H, Kim D-Y, Kim J-H, Kim Y-M, Kim K-R, Kim Y-T, Nam J-H (2006) Is complete surgical staging necessary in patients with stage I mucinous epithelial ovarian tumors? Gynecol Oncol 103:878–882PubMed
11.
go back to reference Gungorduk K, Asicioglu O, Braicu EI, Almuheimid J, Gokulu SG, Cetinkaya N, Gungor T, Pakay G, Telli EU, Cuylan ZF (2017) The impact of surgical staging on the prognosis of mucinous borderline tumors of the ovaries: a multicenter study. Anticancer Res 37:5609–5616PubMed Gungorduk K, Asicioglu O, Braicu EI, Almuheimid J, Gokulu SG, Cetinkaya N, Gungor T, Pakay G, Telli EU, Cuylan ZF (2017) The impact of surgical staging on the prognosis of mucinous borderline tumors of the ovaries: a multicenter study. Anticancer Res 37:5609–5616PubMed
12.
go back to reference Matsuo K, Machida H, Takiuchi T, Grubbs BH, Roman LD, Sood AK, Gershenson DM (2017) Role of hysterectomy and lymphadenectomy in the management of early-stage borderline ovarian tumors. Gynecol Oncol 144:496–502PubMed Matsuo K, Machida H, Takiuchi T, Grubbs BH, Roman LD, Sood AK, Gershenson DM (2017) Role of hysterectomy and lymphadenectomy in the management of early-stage borderline ovarian tumors. Gynecol Oncol 144:496–502PubMed
13.
go back to reference Camatte S, Morice P, Atallah D, Pautier P, Lhomme C, Haie-Meder C, Duvillard P, Castaigne D (2002) Lymph node disorders and prognostic value of nodal involvement in patients treated for a borderline ovarian tumor: an analysis of a series of 42 lymphadenectomies. J Am Coll Surg 195:332–338PubMed Camatte S, Morice P, Atallah D, Pautier P, Lhomme C, Haie-Meder C, Duvillard P, Castaigne D (2002) Lymph node disorders and prognostic value of nodal involvement in patients treated for a borderline ovarian tumor: an analysis of a series of 42 lymphadenectomies. J Am Coll Surg 195:332–338PubMed
14.
go back to reference Pawlik TM, Gleisner AL, Cameron JL, Winter JM, Assumpcao L, Lillemoe KD, Wolfgang C, Hruban RH, Schulick RD, Yeo CJ, Choti MA (2007) Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer. Surgery 141:610–618PubMed Pawlik TM, Gleisner AL, Cameron JL, Winter JM, Assumpcao L, Lillemoe KD, Wolfgang C, Hruban RH, Schulick RD, Yeo CJ, Choti MA (2007) Prognostic relevance of lymph node ratio following pancreaticoduodenectomy for pancreatic cancer. Surgery 141:610–618PubMed
15.
go back to reference Riediger H, Keck T, Wellner U, Zur Hausen A, Adam U, Hopt UT, Makowiec F (2009) The lymph node ratio is the strongest prognostic factor after resection of pancreatic cancer. J Gastrointest Surg 13:1337PubMed Riediger H, Keck T, Wellner U, Zur Hausen A, Adam U, Hopt UT, Makowiec F (2009) The lymph node ratio is the strongest prognostic factor after resection of pancreatic cancer. J Gastrointest Surg 13:1337PubMed
16.
go back to reference Rosenberg R, Friederichs J, Schuster T, Gertler R, Maak M, Becker K, Grebner A, Ulm K, Höfler H, Nekarda H (2008) Prognosis of patients with colorectal cancer is associated with lymph node ratio: a single-center analysis of 3026 patients over a 25-year time period. Ann Surg 248:968–978PubMed Rosenberg R, Friederichs J, Schuster T, Gertler R, Maak M, Becker K, Grebner A, Ulm K, Höfler H, Nekarda H (2008) Prognosis of patients with colorectal cancer is associated with lymph node ratio: a single-center analysis of 3026 patients over a 25-year time period. Ann Surg 248:968–978PubMed
17.
go back to reference Rosenberg R, Engel J, Bruns C, Heitland W, Hermes N, Jauch K-W, Kopp R, Pütterich E, Ruppert R, Schuster T (2010) The prognostic value of lymph node ratio in a population-based collective of colorectal cancer patients. Ann Surg 251:1070–1078PubMed Rosenberg R, Engel J, Bruns C, Heitland W, Hermes N, Jauch K-W, Kopp R, Pütterich E, Ruppert R, Schuster T (2010) The prognostic value of lymph node ratio in a population-based collective of colorectal cancer patients. Ann Surg 251:1070–1078PubMed
18.
go back to reference Schneider DF, Chen H, Sippel RS (2013) Impact of lymph node ratio on survival in papillary thyroid cancer. Ann Surg Oncol 20:1906–1911PubMed Schneider DF, Chen H, Sippel RS (2013) Impact of lymph node ratio on survival in papillary thyroid cancer. Ann Surg Oncol 20:1906–1911PubMed
19.
go back to reference Van der Wal B, Butzelaar R, Van der Meij S, Boermeester M (2002) Axillary lymph node ratio and total number of removed lymph nodes: predictors of survival in stage I and II breast cancer. Eur J Surg Oncol 28:481–489PubMed Van der Wal B, Butzelaar R, Van der Meij S, Boermeester M (2002) Axillary lymph node ratio and total number of removed lymph nodes: predictors of survival in stage I and II breast cancer. Eur J Surg Oncol 28:481–489PubMed
20.
go back to reference Voordeckers M, Vinh-Hung V, Van de Steene J, Lamote J, Storme G (2004) The lymph node ratio as prognostic factor in node-positive breast cancer. Radiother Oncol 70:225–230PubMed Voordeckers M, Vinh-Hung V, Van de Steene J, Lamote J, Storme G (2004) The lymph node ratio as prognostic factor in node-positive breast cancer. Radiother Oncol 70:225–230PubMed
21.
go back to reference Liu Y, Ma L, Wang S, Chen Y, Wu G, Han M, Wang X (2010) Prognostic value of lymph node metastases and lymph node ratio in esophageal squamous cell carcinoma. Eur J Surg Oncol 36:155–159PubMed Liu Y, Ma L, Wang S, Chen Y, Wu G, Han M, Wang X (2010) Prognostic value of lymph node metastases and lymph node ratio in esophageal squamous cell carcinoma. Eur J Surg Oncol 36:155–159PubMed
22.
go back to reference Roder J, Busch R, Stein H, Fink U, Siewert J (1994) Ratio of invaded to removed lymph nodes as a predictor of survival in squamous cell carcinoma of the oesophagus. Br J Surg 81:410–413PubMed Roder J, Busch R, Stein H, Fink U, Siewert J (1994) Ratio of invaded to removed lymph nodes as a predictor of survival in squamous cell carcinoma of the oesophagus. Br J Surg 81:410–413PubMed
23.
go back to reference Nwogu CE, Groman A, Fahey D, Yendamuri S, Dexter E, Demmy TL, Miller A, Reid M (2012) Number of lymph nodes and metastatic lymph node ratio are associated with survival in lung cancer. Ann Thorac Surg 93:1614–1620PubMedPubMedCentral Nwogu CE, Groman A, Fahey D, Yendamuri S, Dexter E, Demmy TL, Miller A, Reid M (2012) Number of lymph nodes and metastatic lymph node ratio are associated with survival in lung cancer. Ann Thorac Surg 93:1614–1620PubMedPubMedCentral
24.
go back to reference Xing Y, Badgwell BD, Ross MI, Gershenwald JE, Lee JE, Mansfield PF, Lucci A, Cormier JN (2009) Lymph node ratio predicts disease-specific survival in melanoma patients. Cancer 115:2505–2513PubMedPubMedCentral Xing Y, Badgwell BD, Ross MI, Gershenwald JE, Lee JE, Mansfield PF, Lucci A, Cormier JN (2009) Lymph node ratio predicts disease-specific survival in melanoma patients. Cancer 115:2505–2513PubMedPubMedCentral
25.
go back to reference Chan J, Kapp D, Cheung M, Osann K, Shin J, Cohn D, Seid P (2007) The impact of the absolute number and ratio of positive lymph nodes on survival of endometrioid uterine cancer patients. Br J Cancer 97:605–611PubMedPubMedCentral Chan J, Kapp D, Cheung M, Osann K, Shin J, Cohn D, Seid P (2007) The impact of the absolute number and ratio of positive lymph nodes on survival of endometrioid uterine cancer patients. Br J Cancer 97:605–611PubMedPubMedCentral
26.
go back to reference Fleming ND, Frumovitz M, Schmeler KM, dos Reis R, Munsell MF, Eifel PJ, Soliman PT, Nick AM, Westin SN, Ramirez PT (2015) Significance of lymph node ratio in defining risk category in node-positive early stage cervical cancer. Gynecol Oncol 136:48–53PubMed Fleming ND, Frumovitz M, Schmeler KM, dos Reis R, Munsell MF, Eifel PJ, Soliman PT, Nick AM, Westin SN, Ramirez PT (2015) Significance of lymph node ratio in defining risk category in node-positive early stage cervical cancer. Gynecol Oncol 136:48–53PubMed
27.
go back to reference Polterauer S, Schwameis R, Grimm C, Macuks R, Iacoponi S, Zalewski K, Zapardiel I, Group VSC (2017) Prognostic value of lymph node ratio and number of positive inguinal nodes in patients with vulvar cancer. Gynecol Oncol 147:92–97PubMed Polterauer S, Schwameis R, Grimm C, Macuks R, Iacoponi S, Zalewski K, Zapardiel I, Group VSC (2017) Prognostic value of lymph node ratio and number of positive inguinal nodes in patients with vulvar cancer. Gynecol Oncol 147:92–97PubMed
28.
go back to reference Polterauer S, Schwameis R, Grimm C, Hillemanns P, Juckstock J, Hilpert F, de Gregorio N, Hasenburg A, Sehouli J, Furst ST, Strauss HG, Baumann K, Thiel F, Mustea A, Harter P, Wimberger P, Kolbl H, Reinthaller A, Woelber L, Mahner S (2019) Lymph node ratio in inguinal lymphadenectomy for squamous cell vulvar cancer: results from the AGO-CaRE-1 study. Gynecol Oncol 153:286–291PubMed Polterauer S, Schwameis R, Grimm C, Hillemanns P, Juckstock J, Hilpert F, de Gregorio N, Hasenburg A, Sehouli J, Furst ST, Strauss HG, Baumann K, Thiel F, Mustea A, Harter P, Wimberger P, Kolbl H, Reinthaller A, Woelber L, Mahner S (2019) Lymph node ratio in inguinal lymphadenectomy for squamous cell vulvar cancer: results from the AGO-CaRE-1 study. Gynecol Oncol 153:286–291PubMed
29.
go back to reference Ayhan A, Ozkan NT, Sari ME, Celik H, Dede M, Akbayir O, Gungorduk K, Sahin H, Haberal A, Gungor T, Arvas M, Meydanli MM (2018) Impact of lymph node ratio on survival in stage III ovarian high-grade serous cancer: a Turkish Gynecologic Oncology Group study. J Gynecol Oncol 29:e12PubMed Ayhan A, Ozkan NT, Sari ME, Celik H, Dede M, Akbayir O, Gungorduk K, Sahin H, Haberal A, Gungor T, Arvas M, Meydanli MM (2018) Impact of lymph node ratio on survival in stage III ovarian high-grade serous cancer: a Turkish Gynecologic Oncology Group study. J Gynecol Oncol 29:e12PubMed
30.
go back to reference Zhou J, He ZY, Li FY, Sun JY, Lin HX, Wu SG, Chen QH (2016) Prognostic value of lymph node ratio in stage IIIC epithelial ovarian cancer with node-positive in a SEER population-based study. Oncotarget 7:7952–7959PubMedPubMedCentral Zhou J, He ZY, Li FY, Sun JY, Lin HX, Wu SG, Chen QH (2016) Prognostic value of lymph node ratio in stage IIIC epithelial ovarian cancer with node-positive in a SEER population-based study. Oncotarget 7:7952–7959PubMedPubMedCentral
33.
go back to reference Matsuo K, Machida H, Mandelbaum RS, Grubbs BH, Roman LD, Sood AK, Gershenson DM (2019) Mucinous borderline ovarian tumor versus invasive well-differentiated mucinous ovarian cancer: difference in characteristics and outcomes. Gynecol Oncol 153:230–237PubMed Matsuo K, Machida H, Mandelbaum RS, Grubbs BH, Roman LD, Sood AK, Gershenson DM (2019) Mucinous borderline ovarian tumor versus invasive well-differentiated mucinous ovarian cancer: difference in characteristics and outcomes. Gynecol Oncol 153:230–237PubMed
34.
go back to reference Matsuo K, Shimada M, Yamaguchi S, Matoda M, Nakanishi T, Kikkawa F, Ohmichi M, Okamoto A, Sugiyama T, Mikami M (2019) Association of radical hysterectomy surgical volume and survival of women with early-stage cervical cancer. Obstet Gynecol 133:1086–1098PubMed Matsuo K, Shimada M, Yamaguchi S, Matoda M, Nakanishi T, Kikkawa F, Ohmichi M, Okamoto A, Sugiyama T, Mikami M (2019) Association of radical hysterectomy surgical volume and survival of women with early-stage cervical cancer. Obstet Gynecol 133:1086–1098PubMed
35.
go back to reference McCluggage WG (2010) The pathology of and controversial aspects of ovarian borderline tumours. Curr Opin Oncol 22:462–472PubMed McCluggage WG (2010) The pathology of and controversial aspects of ovarian borderline tumours. Curr Opin Oncol 22:462–472PubMed
36.
go back to reference Matsuo K, Machida H, Mariani A, Mandelbaum RS, Glaser GE, Gostout BS, Roman LD, Wright JD (2018) Adequate pelvic lymphadenectomy and survival of women with early-stage epithelial ovarian cancer. J Gynecol Oncol 29:e69PubMedPubMedCentral Matsuo K, Machida H, Mariani A, Mandelbaum RS, Glaser GE, Gostout BS, Roman LD, Wright JD (2018) Adequate pelvic lymphadenectomy and survival of women with early-stage epithelial ovarian cancer. J Gynecol Oncol 29:e69PubMedPubMedCentral
37.
go back to reference Morgan RJ, Armstrong DK, Alvarez RD, Bakkum-Gamez JN, Behbakht K, Chen L-M, Copeland L, Crispens MA, DeRosa M, Dorigo O (2016) Ovarian cancer, version 1.2016, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 14:1134–1163PubMed Morgan RJ, Armstrong DK, Alvarez RD, Bakkum-Gamez JN, Behbakht K, Chen L-M, Copeland L, Crispens MA, DeRosa M, Dorigo O (2016) Ovarian cancer, version 1.2016, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw 14:1134–1163PubMed
38.
go back to reference Shazly SA, Laughlin-Tommaso SK, Dowdy SC, Famuyide AO (2016) Staging for low malignant potential ovarian tumors: a global perspective. Am J Obstet Gynecol 215:153–168e2PubMed Shazly SA, Laughlin-Tommaso SK, Dowdy SC, Famuyide AO (2016) Staging for low malignant potential ovarian tumors: a global perspective. Am J Obstet Gynecol 215:153–168e2PubMed
39.
go back to reference du Bois A, Ewald-Riegler N, de Gregorio N, Reuss A, Mahner S, Fotopoulou C, Kommoss F, Schmalfeldt B, Hilpert F, Fehm T, Burges A, Meier W, Hillemanns P, Hanker L, Hasenburg A, Strauss HG, Hellriegel M, Wimberger P, Keyver-Paik MD, Baumann K, Canzler U, Wollschlaeger K, Forner D, Pfisterer J, Schroder W, Munstedt K, Richter B, Kommoss S, Hauptmann S, Arbeitsgmeinschaft Gynakologische Onkologie Study G (2013) Borderline tumours of the ovary: a cohort study of the Arbeitsgmeinschaft Gynakologische Onkologie (AGO) Study Group. Eur J Cancer 49:1905–1914PubMed du Bois A, Ewald-Riegler N, de Gregorio N, Reuss A, Mahner S, Fotopoulou C, Kommoss F, Schmalfeldt B, Hilpert F, Fehm T, Burges A, Meier W, Hillemanns P, Hanker L, Hasenburg A, Strauss HG, Hellriegel M, Wimberger P, Keyver-Paik MD, Baumann K, Canzler U, Wollschlaeger K, Forner D, Pfisterer J, Schroder W, Munstedt K, Richter B, Kommoss S, Hauptmann S, Arbeitsgmeinschaft Gynakologische Onkologie Study G (2013) Borderline tumours of the ovary: a cohort study of the Arbeitsgmeinschaft Gynakologische Onkologie (AGO) Study Group. Eur J Cancer 49:1905–1914PubMed
40.
go back to reference Boyraz G, Salman MC, Gultekin M, Ozkan NT, Uckan HH, Gungorduk K, Gulseren V, Ayik H, Toptas T, Kuru O, Sozen H, Erturk A, Ozgul N, Meydanlı MM, Sanci M, Turan T, Gungor T, Simsek T, Topuz S, Yuce K (2017) What is the impact of stromal microinvasion on oncologic outcomes in borderline ovarian tumors? A multicenter case-control study. Arch Gynecol Obstet 296(5):979–987PubMed Boyraz G, Salman MC, Gultekin M, Ozkan NT, Uckan HH, Gungorduk K, Gulseren V, Ayik H, Toptas T, Kuru O, Sozen H, Erturk A, Ozgul N, Meydanlı MM, Sanci M, Turan T, Gungor T, Simsek T, Topuz S, Yuce K (2017) What is the impact of stromal microinvasion on oncologic outcomes in borderline ovarian tumors? A multicenter case-control study. Arch Gynecol Obstet 296(5):979–987PubMed
41.
go back to reference Du Bois A, Ewald-Riegler N, Du Bois O, Harter P (2009) Borderlinetumoren des Ovars—eine systematische Übersicht. Borderline tumors of the ovary—a systematic review. Geburtshilfe Frauenheilkd 69:1–27 Du Bois A, Ewald-Riegler N, Du Bois O, Harter P (2009) Borderlinetumoren des Ovars—eine systematische Übersicht. Borderline tumors of the ovary—a systematic review. Geburtshilfe Frauenheilkd 69:1–27
42.
go back to reference Kurman RJ, Carcangiu ML, Herrington CS, Young RH (2014) WHO classification of tumours of female reproductive organs, 4th edn. IARC International Agency for Research on Cancer, Lyon, pp 10–40 Kurman RJ, Carcangiu ML, Herrington CS, Young RH (2014) WHO classification of tumours of female reproductive organs, 4th edn. IARC International Agency for Research on Cancer, Lyon, pp 10–40
43.
go back to reference Matsuo K, Machida H, Grubbs BH, Matsuzaki S, Klar M, Roman LD, Sood AK, Gershenson DM (2020) Diagnosis-shift between low-grade serous ovarian cancer and serous borderline ovarian tumor: A population-based study. Gynecol Oncol 157(1):21–28PubMed Matsuo K, Machida H, Grubbs BH, Matsuzaki S, Klar M, Roman LD, Sood AK, Gershenson DM (2020) Diagnosis-shift between low-grade serous ovarian cancer and serous borderline ovarian tumor: A population-based study. Gynecol Oncol 157(1):21–28PubMed
Metadata
Title
Significance of lymph node ratio on survival of women with borderline ovarian tumors
Authors
David J. Nusbaum
Rachel S. Mandelbaum
Hiroko Machida
Shinya Matsuzaki
Lynda D. Roman
Anil K. Sood
David M. Gershenson
Koji Matsuo
Publication date
01-05-2020
Publisher
Springer Berlin Heidelberg
Published in
Archives of Gynecology and Obstetrics / Issue 5/2020
Print ISSN: 0932-0067
Electronic ISSN: 1432-0711
DOI
https://doi.org/10.1007/s00404-020-05535-0

Other articles of this Issue 5/2020

Archives of Gynecology and Obstetrics 5/2020 Go to the issue