Ovarian serous tumors of low malignant potential (borderline tumors): Outcome-based study of 276 patients with long-term (≥5-year) follow-up

Teri A. Longacre, Jesse K. McKenney, Henry D. Tazelaar, Richard L. Kempson, Michael R. Hendrickson

Research output: Contribution to journalArticle

209 Citations (Scopus)

Abstract

The natural history, classification, and nomenclature of ovarian serous tumors of low malignant potential (S-LMP) (serous tumors of borderline malignancy, atypical proliferating tumors) are controversial. To determine long-term outcome for patients with S-LMP and further evaluate whether S-LMP can be stratified into clinically benign and malignant groups, the clinicopathologic features of 276 patients with S-LMP and ≥5 year follow-up were studied. The histology of the ovarian primary, extraovarian implants, and recurrent tumor(s) were characterized using World Health Organization criteria and correlated with FIGO stage and clinical follow-up. After censoring nontumor deaths, overall survival and disease-free survival for the 276 patients was 95% (98% FIGO stage I; 91% FIGO II-IV) and 78% (87% FIGO stage I; 65% FIGO stage II-IV), respectively. Unresectable disease (P < 0.001) and invasive implants (P < 0.001) were associated with decreased survival. When compared with typical S-LMP, S-LMP with micropapillary features were more strongly associated with invasive implants (P < 0.008) and decreased overall survival (P = 0.004), but patient outcome with micropapillary S-LMP was not independent of implant type. Stromal microinvasion in the primary tumor was also correlated with adverse outcome, independent of stage of disease, micropapillary architecture, and implant type (P = 0.03). There was no association between outcome and lymph node status. Transformation to low-grade serous carcinoma occurred in 6.8% of patients at intervals of 7 to 288 months (58% ≥ 60 months) and was strongly associated with increased tempo of disease and decreased survival (P < 0.001). S-LMP forms a heterogeneous group, morphologically and clinically distinct from benign serous tumors and serous carcinoma. The majority of S-LMP are clinically benign, but recurrences are not uncommon, and persistent disease as well as deaths occur. Progression to low-grade serous carcinoma is highly predictive of more aggressive disease. Other features associated with recurrent and/or progressive disease include FIGO stage, invasive implants, microinvasion in the primary tumor, and micropapillary architecture. These predictors tend to co-occur, and no single clinical or pathologic feature or combination of features identify all adverse outcomes. The small, but significant risk of progression over time to low-grade serous carcinoma emphasizes the need for prolonged follow-up in patients with S-LMP.

Original languageEnglish (US)
Pages (from-to)707-723
Number of pages17
JournalAmerican Journal of Surgical Pathology
Volume29
Issue number6
DOIs
StatePublished - Jun 2005

Fingerprint

Outcome Assessment (Health Care)
Neoplasms
Carcinoma
Survival
Natural History
Terminology
Disease-Free Survival
Histology
Lymph Nodes
Recurrence

Keywords

  • Atypical proliferating tumor
  • Borderline tumor
  • Invasive implant
  • Micro-invasion
  • Micropapillary
  • Serous tumor of low malignant potential

ASJC Scopus subject areas

  • Anatomy
  • Pathology and Forensic Medicine

Cite this

Ovarian serous tumors of low malignant potential (borderline tumors) : Outcome-based study of 276 patients with long-term (≥5-year) follow-up. / Longacre, Teri A.; McKenney, Jesse K.; Tazelaar, Henry D.; Kempson, Richard L.; Hendrickson, Michael R.

In: American Journal of Surgical Pathology, Vol. 29, No. 6, 06.2005, p. 707-723.

Research output: Contribution to journalArticle

Longacre, Teri A. ; McKenney, Jesse K. ; Tazelaar, Henry D. ; Kempson, Richard L. ; Hendrickson, Michael R. / Ovarian serous tumors of low malignant potential (borderline tumors) : Outcome-based study of 276 patients with long-term (≥5-year) follow-up. In: American Journal of Surgical Pathology. 2005 ; Vol. 29, No. 6. pp. 707-723.
@article{26bac932a5dc4810b9afe68d2a65f551,
title = "Ovarian serous tumors of low malignant potential (borderline tumors): Outcome-based study of 276 patients with long-term (≥5-year) follow-up",
abstract = "The natural history, classification, and nomenclature of ovarian serous tumors of low malignant potential (S-LMP) (serous tumors of borderline malignancy, atypical proliferating tumors) are controversial. To determine long-term outcome for patients with S-LMP and further evaluate whether S-LMP can be stratified into clinically benign and malignant groups, the clinicopathologic features of 276 patients with S-LMP and ≥5 year follow-up were studied. The histology of the ovarian primary, extraovarian implants, and recurrent tumor(s) were characterized using World Health Organization criteria and correlated with FIGO stage and clinical follow-up. After censoring nontumor deaths, overall survival and disease-free survival for the 276 patients was 95{\%} (98{\%} FIGO stage I; 91{\%} FIGO II-IV) and 78{\%} (87{\%} FIGO stage I; 65{\%} FIGO stage II-IV), respectively. Unresectable disease (P < 0.001) and invasive implants (P < 0.001) were associated with decreased survival. When compared with typical S-LMP, S-LMP with micropapillary features were more strongly associated with invasive implants (P < 0.008) and decreased overall survival (P = 0.004), but patient outcome with micropapillary S-LMP was not independent of implant type. Stromal microinvasion in the primary tumor was also correlated with adverse outcome, independent of stage of disease, micropapillary architecture, and implant type (P = 0.03). There was no association between outcome and lymph node status. Transformation to low-grade serous carcinoma occurred in 6.8{\%} of patients at intervals of 7 to 288 months (58{\%} ≥ 60 months) and was strongly associated with increased tempo of disease and decreased survival (P < 0.001). S-LMP forms a heterogeneous group, morphologically and clinically distinct from benign serous tumors and serous carcinoma. The majority of S-LMP are clinically benign, but recurrences are not uncommon, and persistent disease as well as deaths occur. Progression to low-grade serous carcinoma is highly predictive of more aggressive disease. Other features associated with recurrent and/or progressive disease include FIGO stage, invasive implants, microinvasion in the primary tumor, and micropapillary architecture. These predictors tend to co-occur, and no single clinical or pathologic feature or combination of features identify all adverse outcomes. The small, but significant risk of progression over time to low-grade serous carcinoma emphasizes the need for prolonged follow-up in patients with S-LMP.",
keywords = "Atypical proliferating tumor, Borderline tumor, Invasive implant, Micro-invasion, Micropapillary, Serous tumor of low malignant potential",
author = "Longacre, {Teri A.} and McKenney, {Jesse K.} and Tazelaar, {Henry D.} and Kempson, {Richard L.} and Hendrickson, {Michael R.}",
year = "2005",
month = "6",
doi = "10.1097/01.pas.0000164030.82810.db",
language = "English (US)",
volume = "29",
pages = "707--723",
journal = "American Journal of Surgical Pathology",
issn = "0147-5185",
publisher = "Lippincott Williams and Wilkins",
number = "6",

}

TY - JOUR

T1 - Ovarian serous tumors of low malignant potential (borderline tumors)

T2 - Outcome-based study of 276 patients with long-term (≥5-year) follow-up

AU - Longacre, Teri A.

AU - McKenney, Jesse K.

AU - Tazelaar, Henry D.

AU - Kempson, Richard L.

AU - Hendrickson, Michael R.

PY - 2005/6

Y1 - 2005/6

N2 - The natural history, classification, and nomenclature of ovarian serous tumors of low malignant potential (S-LMP) (serous tumors of borderline malignancy, atypical proliferating tumors) are controversial. To determine long-term outcome for patients with S-LMP and further evaluate whether S-LMP can be stratified into clinically benign and malignant groups, the clinicopathologic features of 276 patients with S-LMP and ≥5 year follow-up were studied. The histology of the ovarian primary, extraovarian implants, and recurrent tumor(s) were characterized using World Health Organization criteria and correlated with FIGO stage and clinical follow-up. After censoring nontumor deaths, overall survival and disease-free survival for the 276 patients was 95% (98% FIGO stage I; 91% FIGO II-IV) and 78% (87% FIGO stage I; 65% FIGO stage II-IV), respectively. Unresectable disease (P < 0.001) and invasive implants (P < 0.001) were associated with decreased survival. When compared with typical S-LMP, S-LMP with micropapillary features were more strongly associated with invasive implants (P < 0.008) and decreased overall survival (P = 0.004), but patient outcome with micropapillary S-LMP was not independent of implant type. Stromal microinvasion in the primary tumor was also correlated with adverse outcome, independent of stage of disease, micropapillary architecture, and implant type (P = 0.03). There was no association between outcome and lymph node status. Transformation to low-grade serous carcinoma occurred in 6.8% of patients at intervals of 7 to 288 months (58% ≥ 60 months) and was strongly associated with increased tempo of disease and decreased survival (P < 0.001). S-LMP forms a heterogeneous group, morphologically and clinically distinct from benign serous tumors and serous carcinoma. The majority of S-LMP are clinically benign, but recurrences are not uncommon, and persistent disease as well as deaths occur. Progression to low-grade serous carcinoma is highly predictive of more aggressive disease. Other features associated with recurrent and/or progressive disease include FIGO stage, invasive implants, microinvasion in the primary tumor, and micropapillary architecture. These predictors tend to co-occur, and no single clinical or pathologic feature or combination of features identify all adverse outcomes. The small, but significant risk of progression over time to low-grade serous carcinoma emphasizes the need for prolonged follow-up in patients with S-LMP.

AB - The natural history, classification, and nomenclature of ovarian serous tumors of low malignant potential (S-LMP) (serous tumors of borderline malignancy, atypical proliferating tumors) are controversial. To determine long-term outcome for patients with S-LMP and further evaluate whether S-LMP can be stratified into clinically benign and malignant groups, the clinicopathologic features of 276 patients with S-LMP and ≥5 year follow-up were studied. The histology of the ovarian primary, extraovarian implants, and recurrent tumor(s) were characterized using World Health Organization criteria and correlated with FIGO stage and clinical follow-up. After censoring nontumor deaths, overall survival and disease-free survival for the 276 patients was 95% (98% FIGO stage I; 91% FIGO II-IV) and 78% (87% FIGO stage I; 65% FIGO stage II-IV), respectively. Unresectable disease (P < 0.001) and invasive implants (P < 0.001) were associated with decreased survival. When compared with typical S-LMP, S-LMP with micropapillary features were more strongly associated with invasive implants (P < 0.008) and decreased overall survival (P = 0.004), but patient outcome with micropapillary S-LMP was not independent of implant type. Stromal microinvasion in the primary tumor was also correlated with adverse outcome, independent of stage of disease, micropapillary architecture, and implant type (P = 0.03). There was no association between outcome and lymph node status. Transformation to low-grade serous carcinoma occurred in 6.8% of patients at intervals of 7 to 288 months (58% ≥ 60 months) and was strongly associated with increased tempo of disease and decreased survival (P < 0.001). S-LMP forms a heterogeneous group, morphologically and clinically distinct from benign serous tumors and serous carcinoma. The majority of S-LMP are clinically benign, but recurrences are not uncommon, and persistent disease as well as deaths occur. Progression to low-grade serous carcinoma is highly predictive of more aggressive disease. Other features associated with recurrent and/or progressive disease include FIGO stage, invasive implants, microinvasion in the primary tumor, and micropapillary architecture. These predictors tend to co-occur, and no single clinical or pathologic feature or combination of features identify all adverse outcomes. The small, but significant risk of progression over time to low-grade serous carcinoma emphasizes the need for prolonged follow-up in patients with S-LMP.

KW - Atypical proliferating tumor

KW - Borderline tumor

KW - Invasive implant

KW - Micro-invasion

KW - Micropapillary

KW - Serous tumor of low malignant potential

UR - http://www.scopus.com/inward/record.url?scp=19544375061&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=19544375061&partnerID=8YFLogxK

U2 - 10.1097/01.pas.0000164030.82810.db

DO - 10.1097/01.pas.0000164030.82810.db

M3 - Article

C2 - 15897738

AN - SCOPUS:19544375061

VL - 29

SP - 707

EP - 723

JO - American Journal of Surgical Pathology

JF - American Journal of Surgical Pathology

SN - 0147-5185

IS - 6

ER -