Advertisement

Annals of Surgical Oncology

, Volume 22, Issue 11, pp 3695–3700 | Cite as

Microscopic Omental Metastasis in Clinical Stage I Endometrial Cancer: A Meta-analysis

  • Won Duk Joo
  • Peter E. Schwartz
  • Thomas J. Rutherford
  • Seok Ju Seong
  • Junbeom Ku
  • Hyun Park
  • Sang Geun Jung
  • Min Chul Choi
  • Chan Lee
Gynecologic Oncology

Abstract

Background

A patient with early-stage endometrial cancer may possibly have microscopic metastasis in the omentum, which is associated with a poor prognosis. The purpose of this study was to identify risk factors for microscopic omental metastasis in patients with clinical stage I endometrial cancer to establish the indications for selective omentectomy.

Methods

We searched the PubMed, EMBASE, and Cochrane Library databases for published studies from inception to August 2014, using terms such as ‘endometrial cancer’ or ‘uterine cancer’ for disease, ‘omentectomy’ or ‘omental biopsy’ for intervention, and ‘metastasis’ for outcome. Two reviewers independently identified the studies that matched the selection criteria. We calculated the pooled risk ratios (RRs) with 95 % confidence intervals (CI) of each surgicopathologic finding for microscopic omental metastases in clinical stage I endometrial cancer. We also calculated the prevalence of microscopic omental metastases.

Results

Among 1163 patients from ten studies, 22 cases (1.9 %) of microscopic omental metastases were found, which accounted for 26.5 % of all omental metastases. Positive lymph nodes (RR 8.71, 95 % CI 1.38–54.95), adnexal metastases (RR 16.76, 95 % CI 2.60–107.97), and appendiceal implants (RR 161.67, 95 % CI 5.16–5061.03) were highly associated with microscopic omental metastases.

Conclusions

Microscopic omental metastases were not negligible in patients with clinical stage I endometrial cancer. Those with a risk factor of microscopic omental metastases were recommended for selective omentectomy.

Keywords

Endometrial Cancer Clinical Stage Endometrioid Adenocarcinoma Positive Cytology Cochrane Library Database 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Omental metastasis of endometrial cancer implies peritoneal spread of carcinoma and is regarded as advanced (stage IVB) endometrial cancer.1 However, omental metastases may apparently be present in early clinical stage as well as advanced-stage disease. The prevalence of omental metastases has been reported as approximately 3–8 % in patients with clinical stage I endometrial cancer.2 Intraperitoneal spread of endometrial cancer, including omental metastasis, is highly associated with lymph node metastases, as well as recurrence.3,4 Neither omentectomy or omental biopsy are included in the standard staging procedures for endometrial cancer but are recommended in special situations. All guidelines for the treatment of endometrial cancer recommended omentectomy for visible peritoneal dissemination, or in cases of papillary serous or clear cell carcinoma, and carcinosarcoma.5, 6, 7, 8

The majority of endometrial cancer patients are diagnosed without clinical evidence of extrauterine spread [International Federation of Gynecology and Obstetrics (FIGO) stage I and II] and 5-year survival is approximately 90 %;9 however, approximately 10–15 % of patients with early-stage endometrial cancer will experience recurrences.2,3 Why do these patients recur in such early stages? Patients without omentectomy will be understaged if they have microscopic omental metastases, which leads to unexpected poor prognosis. To date, the prevalence of microscopic omental metastases has not been reported. Although inspection is not always accurate, we do not have enough evidence to perform omentectomies in all patients without gross omental implants. It seems reasonable to identify risk factors for microscopic omental metastases, and to selectively perform omentectomies for patients with such a risk factor as part of their initial surgical staging. Therefore, this study aimed to estimate how often microscopic omental metastases occur, and to find out which factors are associated with microscopic omental metastases in patients with clinical stage I endometrial cancer.

Materials and Methods

Literature Search

We followed the Meta-analysis Of Observational Studies in Epidemiology (MOOSE) statement for systematic review and meta-analysis.10 This study was a meta-analysis of published data and therefore did not require Ethics Committee approval. We searched the PubMed, EMBASE, and Cochrane Library databases from inception to August 2014, using keywords related to omentectomy and omental biopsy as surgical procedures of endometrial cancer in both retrospective and prospective studies. We also checked the bibliographies of relevant articles to discover additional literature on this topic. We selected keywords for the literature search, such as ‘endometrial neoplasm’, ‘endometrial cancer’, ‘endometrial carcinoma’, ‘uterine neoplasm’, ‘uterine cancer’, or ‘uterine carcinoma’ for disease; ‘omentectomy’ or ‘omental biopsy’ for intervention; and ‘metastasis’ or ‘metastases’ for outcome (Fig. 1).
Fig. 1

Identification process of relevant studies

Selection Criteria

The selection criteria for relevant studies were as follows: (i) omentectomies or omental biopsies were performed in patients with endometrial cancer; (ii) if the main population of a study was uterine neoplasms other than endometrial cancer, such as uterine sarcoma, the study was excluded; (iii) any type of study design was accepted, whether it was randomized controlled or observational, prospective or retrospective; (iv) only original research was accepted—review articles, case reports, and practice guidelines were excluded; (v) the number of patients who had omental metastases was identified or surgicopathologic factors of the patients who had omental metastases were described, such as depth of myometrial invasion, tumor grade, lymph node metastasis, etc.; (vi) the FIGO staging system was used for diagnosis; and (vii) no language restriction. To eliminate publication bias, we did not restrict the language in which the articles were written. Most of the articles included in our analysis were written in English, and two articles written in Chinese were also reviewed.

Studies Identified

Two reviewers (SJS and JK) independently identified a total of 13 observational studies satisfying our selection criteria (Fig. 1). Two studies were prospective, ten studies were retrospective, and one study was both prospective and retrospective. Three studies exclusively enrolled endometrioid adenocarcinoma; one of these studies was prospective and the other studies were retrospective. The remaining ten studies included endometrioid adenocarcinoma as well as other histological types of endometrial cancer, such as serous carcinoma and clear cell carcinoma (Table 1).
Table 1

Characteristics of the included studies

Author

Number of omentectomies

Country

Language

Design

Study period

Age, years [mean ± SD or median (range)]

Clinical stage

Type of omentectomy

Histology

Ren et al.20

234

China

Chinese

Retrospective

1996–2008

56 (30–85)

I–IV

Omentectomy

276 EM, 39 non-EM (18 UPSC, 6 CC, 7 AS, 5 sarcoma, 1 neuroendocrine, 1 undifferentiated, 1 mixed)

Freij et al.2

248

UK

English

Retrospective

2004–2008

65 (33–93)

I–IV

Biopsy

202 EM, 46 non-EM (20 UPSC, 3 CC, 20 MMMT, 3 sarcoma)

Fujiwara et al.11

134

Japan

English

Prospective

1998–2004

57a (<50 years, 19 %; >50 years, 81 %)

I

Infracolicc/totald

Only EM

Metindir and Dilek13

65

Turkey

English

Retrospective

2002–2005

57.4 ± 8.99 (35–80)

I

Infracolic

Only EM

Usubütün et al.21

124

Turkey

English

Prospective/retrospective

2003–2005

NS

NS

Omentectomy

100 EM, 24 non-EM (7 UPSC, 17 other types, including CC, undifferentiated, carcinosarcoma, and unclassified)

Dilek et al.12

51

Turkey

English

Retrospective

1996–2003

60.45 (38–77)

I

Infracolic

Only EM

Gehrig et al.15

52

USA

English

Retrospective

1990–2000

68 (53–97)

I

Partial/total

Only UPSC

Nieto et al.17

80

UK

English

Prospective

1997–2001

NS

I

Biopsye

92 EM, 8 non-EM (4 UPSC, 3 CC, 1 undifferentiated)

Saygili et al.18

97

Turkey

English

Retrospective

1992–1999

58b (<50 years, 22 %; >50 years, 78 %)

I

Infracolic

76 EM, 21 non-EM (7 UPSC, 5 CC, 7 AS, 2 mucinous)

Zhang et al.19

96

China

Chinese

Retrospective

1995–1999

54.6 (30–76)

I–IV

NS

71 EM, 25 non-EM (2 UPSC, 3 CC, 13 adenosquamous, 5 adenoacanthoma, 2 mucinous)

Larson et al.22

236

USA

English

Retrospective

1987–1995

65.9 ± 11.4

NS

Biopsyf

221 EM, 15 non-EM (10 UPSC, 4 CC, 1 mucinous)

Marino et al.16

228

USA

English

Retrospective

1985–1993

63b (32–88)

I

Biopsy

226 EM, 69 non-EM (41 UPSC, 8 CC, 11 AS, 9 mixed)

Chen and Spiegel14

84

USA

English

Retrospective

1986–1989

NS

I

Biopsyg/totalh

65 EM, 19 non-EM (13 UPSC, 3 CC, 2 AS, 1 secretory)

SD standard deviation, NS not specified, UPSC uterine papillary serous carcinoma, EM endometrioid type, CC clear cell carcinoma, AS adenosquamous, MMMT malignant mixed Müllerian tumor

aMedian

bMean

cAt least 10 × 5 cm was excised

dWhen metastases were macroscopically suspected

eExcision of any macroscopic abnormality. If no anomaly was present, a representative biopsy was obtained

fFrom the most dependent portion of the omentum

gIn an omentum with abnormal appearance, at least 10 × 5 cm of the infracolic portion was removed

hIn cases of a gross omental implant or papillary serous carcinoma

Extraction of Data

From the studies selected, two reviewers (SJS and JK) independently extracted the study identification (first author, year of publication), design and period of each study, age, clinical stage, type of omentectomy, histology, number of patients who received either an omentectomy or omental biopsies, number of patients who had omental metastases, and number of patients with microscopic metastases in the omentum. From three studies, we could extract surgicopathologic results, including lymph node metastases, intraperitoneal metastases (adnexa and appendix), peritoneal washing cytology, depth of myometrial invasion, and histological type and grade. Clinical stage I patients were exclusively enrolled for those surgicopathologic data when a study included stage II or higher patients.

Main Analyses

We calculated the prevalence of overall and microscopic omental metastases and the proportion of microscopic metastases among all omental metastases in clinical stage I endometrial cancer. We also calculated the pooled risk ratios (RRs) with 95 % confidence intervals (CI) of histological grade, positive lymph nodes, deep myometrial invasion (≥1/2), adnexal metastases, positive cytology, and appendiceal implants among the subjects who underwent either omentectomies or omental biopsies.

Statistical Analysis

The Chi square test was applied to compare the prevalence of overall omental metastases, and the Fisher’s exact test was applied to compare the proportion of microscopic metastases. The Mantel–Haenszel method based on a fixed-effects model was mainly used to calculate the pooled RR with 95 % CI. The heterogeneity of included studies was evaluated by the Higgins I 2, and a value >50 % was considered to represent substantial heterogeneity. Publication bias was evaluated using the Begg funnel plot. p values <0.05 were considered to be significant. Review Manager (RevMan) version 5.2 (The Nordic Cochrane Centre, The Cochrane Collaboration, Copenhagen, Denmark) and SPSS version 19 software (IBM Corporation, Armonk, NY, USA) were used for statistical analysis.

Results

Prevalence of Omental Metastases

The literature search revealed our study was the first meta-analysis regarding omental metastases of endometrial cancer. Age, clinical stage, type of omentectomy, and histology of patients enrolled in each study are described in Table 1. A total of 13 studies recorded positive rates of omental metastases.2,11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22 The overall prevalence of omental metastases was calculated as 6.2 % (113/1810), regardless of clinical stage. Nine studies recorded positive rates of omental metastases in clinical stage I and the prevalence was 8.2 % (69/841).11, 12, 13, 14, 15, 16, 17, 18, 19 Among these nine studies, three exclusively included endometrioid type; 11, 12, 13 the prevalence of omental metastases in clinical stage I endometrioid carcinoma was 4.4 % (11/250) in these three studies. In the remaining six studies including non-endometrioid type, the prevalence of omental metastases in clinical stage I was 9.8 % (58/591) 14, 15, 16, 17, 18, 19 which was significantly higher than that of only endometrioid type (p = 0.009, χ 2 test). Among 1163 patients from ten studies, 22 cases of microscopic metastases in the omentum were found from a total of 83 cases of omental metastases (26.5 %).2,11, 12, 13, 14, 15, 16, 17, 18,21 There was no difference in the proportion of microscopic metastases, whether the studies included non-endometrioid type or not [26.5 % (18/68) vs. 26.7 % (4/15), p = 1.00, Fisher’s exact test).

Risk Factors for Microscopic Omental Metastasis

We analyzed six items of risk factors that we were able to extract from three studies. Two studies enrolled clinical stage I endometrioid adenocarcinoma exclusively.11,12 The analyzed factors were histological grade, positive lymph nodes, positive cytology, deep myometrial invasion, adnexal metastases, and appendiceal implants. In terms of RR, positive lymph nodes (RR 8.71, 95 % CI 1.38–54.95; I 2 = 0 %),11,12 adnexal metastases (RR 16.76, 95 % CI 2.60–107.97; I 2 = 6 %),11,12 and appendiceal implants (RR 161.67, 95 % CI 5.16–5061.03)12 were significant. Positive cytology,11 deep myometrial invasion,11,12 and histological grade 2,11,12 were not significant (Table 2; Electronic Supplementary Fig. 1s).
Table 2

Pooled risk ratios of the risk factors for microscopic omental metastases and heterogeneity analysis

Factors

No. of analyzed studies

No. of patients (mets/total)

Risk ratio (95 % CI)

Overall effect (p value)

Heterogeneity [I 2] (%)

Grade 3

3

5/425

2.46 (0.54–11.21)

0.25

9

Grade 2 or higher

3

5/425

0.88 (0.17–4.61)

0.88

0

Positive lymph nodes

2

3/177

8.71 (1.38–54.95)

0.02

0

Adnexal metastases

2

3/182

16.76 (2.60–107.97)

0.003

6

Positive cytology

1

1/130

3.43 (0.13–89.24)

0.46

NA

Myometrial invasion ≥½

2

4/182

3.70 (0.60–22.98)

0.16

15

Appendiceal implants

1

3/51

161.67 (5.16–5061.03)

0.004

NA

CI confidence interval, NA not applicable

Heterogeneity and Publication Bias

Heterogeneity analysis demonstrated that there was no significant interstudy variation (I 2, range 0–15 %) (Table 2). Furthermore, the funnel plots for three eligible studies in this meta-analysis revealed that all studies lay inside the funnels with symmetric distribution, suggesting no publication bias in the meta-analysis (Electronic Supplementary Fig. 2s).

Discussion

Peritoneal spread is significantly associated with recurrence and has an important prognostic value. In clinical stage I endometrial cancer, the 5-year disease-free survival rate for patients with non-lymphatic extrauterine disease was 50 % compared with 88 % in the other patients.4 Assessing peritoneal spread requires an omentectomy, as well as peritoneal washing cytology and peritoneal biopsies, as is undertaken in patients with ovarian cancer for staging. Approximately 10 % of patients with clinical stage I endometrial cancer will have pelvic lymph node metastases, and approximately 6 % will have paraaortic lymph node metastases.9 These values are similar to the prevalence of omental metastases in patients with clinical stage I endometrial cancer, which was 8.2 % in our study. Should an omentectomy not be performed for its comparable prognostic value as well as similar positivity compared with lymph node metastases in clinical stage I endometrial cancer? Omentectomy is not a complicated procedure. Its surgical procedure is simple and it does not increase morbidity.17 The specimen is easily extracted through the vagina in case of robotic or laparoscopic surgery. Actually a survey showed that more than half of gynecologic oncologists performed an omentectomy in early-stage endometrial cancer.23 Careful inspection of the omentum is the most important step in detecting tiny omental metastases;21 however, we may fail to notice microscopic metastases if an omentectomy is only performed in cases of gross omental implants. Because 26.5 % of omental metastases were microscopic in our analysis, it is not always reasonable to decide on a patient’s omentectomy by inspection alone. Instead, a selective omentectomy by risk assessment will be helpful in improving the accuracy for detecting omental metastases if no gross implants are visible.

How much sampling is adequate for microscopic examination? Should it be an omental biopsy, an infracolic omentectomy, or a total omentectomy? Table 1 shows the strategy of each previous study. Fujiwara et al. excised at least 10 × 5 cm at the infracolic portion of the omentum in all patients, and performed complete omentectomy if omental metastases were macroscopically suspected.11 This strategy seems the most acceptable. Also, how should the pathologic evaluation be performed? Usubütün et al. noted that one section was sufficient for gross tumor and that three to five samples seemed sufficient for staging if a macroscopic lesion was not detectable and the patient had a high-grade tumor that would necessitate adjuvant therapy.21 This strategy of pathologic evaluation can also be applied to patients who have risk factors for microscopic omental metastases from our analysis.

Patients with omental metastases are expected to have a very poor prognosis. Therefore, a potent adjuvant therapy is necessary. In a series of studies, local recurrence decreased in patients who had adjuvant radiation, but the overall survival was not improved.24 Adjuvant radiation was able to control recurrence in the pelvic cavity but could not block the routes of tumor spread, which were lymph node metastasis and peritoneal spread. Recently, chemotherapy in combination with radiation therapy is being introduced to patients at high risk for recurrence.25 In this regard, omentectomy will provide more information regarding both disease extent and the risk of recurrence, which leads us to choose an appropriate adjuvant therapy. In terms of therapeutic effect, comprehensive staging surgery including omentectomy was reported to improve survival of patients with stage I non-invasive and minimally invasive serous uterine carcinoma.26 Although the omentum may have the ability to trap cancer cells and to destroy them, the ability was not enough to prevent peritoneal tumor outgrowth in a rat model, which supported omentectomy in minimal residual disease.27 Therefore, omentectomy may play a role in improving survival because microscopic omental metastases can be treated by omentectomy.

Most of the studies included in this meta-analysis were retrospective, with the exception of two prospective trials. Selection bias may have occurred if more suspicious patients were enrolled in the retrospective studies. Although the funnel plots suggested no publication bias in this meta-analysis, the small number of the included studies with a small sample size would be prone to publication bias. Therefore, it is necessary to validate our model to predict the risk of microscopic omental metastases in a large-scale, prospective trial to eliminate these potential biases. Besides the diagnostic value of omentectomy, a therapeutic value of omentectomy in high-risk, early-stage endometrial cancer should be evaluated in a future randomized controlled trial.

Conclusions

Our meta-analysis clarified risk factors for microscopic omental metastases in clinical stage I endometrioid adenocarcinoma. Microscopic omental metastases were not negligible in patients with clinical stage I endometrial cancer. Those with a risk factor of microscopic omental metastases would be recommended for selective omentectomy.

Notes

Acknowledgment

This study was supported by a grant from the Korea Healthcare Technology R&D Project, Ministry of Health and Welfare, Republic of Korea (A070001). The study was presented as a poster abstract at the Society of Gynecologic Oncology 44th Annual Meeting on Women’s Cancer, Los Angeles, CA, USA, on 10 March 2013.

Disclosure

Won Duk Joo, Peter E. Schwartz, Thomas J. Rutherford, Seok Ju Seong, Junbeom Ku, Hyun Park, Sang Geun Jung, Min Chul Choi, and Chan Lee report no conflicts of interest.

Supplementary material

10434_2015_4443_MOESM1_ESM.eps (3.3 mb)
Supplementary Fig. 1s Forest plots, the risk of microscopic omental metastases and (a) positive lymph nodes; (b) adnexal metastases; (c) appendiceal implants; (d) positive cytology; (e) deep myometrial invasion (≥1/2); (f) histological grade 3 versus grade 1 and 2; (g) histological grade 3 and 2 versus grade 1. LN, lymph node; MM, myometrial. Supplementary material 1 (EPS 3368 kb)
10434_2015_4443_MOESM2_ESM.eps (149 kb)
Supplementary Fig. 2s Funnel plots of studies included in the meta-analysis of the risk of microscopic omental metastases and (a) positive lymph nodes; (b) adnexal metastases; (c) deep myometrial invasion (≥1/2); (d) histological grade 3 versus grade 1 and 2; (e) histological grade 3 and 2 versus grade 1. All studies lay inside the funnels with symmetric distribution, suggesting no publication bias in the meta-analysis. LN, lymph node; MM, myometrial Supplementary material 2 (EPS 148 kb)

References

  1. 1.
    Pecorelli S. Revised FIGO staging for carcinoma of the vulva, cervix, and endometrium. Int J Gynaecol Obstet. 2009;105:103–4.CrossRefPubMedGoogle Scholar
  2. 2.
    Freij M, Burbos N, Mukhopadhyay D, Lonsdale R, Crocker S, Nieto J. The role of omental biopsy in endometrial cancer staging. Gynecol Surg. 2009;6:251–53.CrossRefGoogle Scholar
  3. 3.
    Creasman WT, Morrow CP, Bundy BN, Homesley HD, Graham JE, Heller PB. Surgical pathologic spread patterns of endometrial cancer. A Gynecologic Oncology Group Study. Cancer. 1987;60:2035–41.CrossRefPubMedGoogle Scholar
  4. 4.
    Lurain JR, Rice BL, Rademaker AW, Poggensee LE, Schink JC, Miller DS. Prognostic factors associated with recurrence in clinical stage I adenocarcinoma of the endometrium. Obstet Gynecol. 1991;78:63–9.PubMedGoogle Scholar
  5. 5.
    National Comprehensive Cancer Network. Uterine neoplasms. NCCN clinical practice guidelines in oncology. Fort Washington (PA): National Comprehensive Cancer Network, Inc., 2012.Google Scholar
  6. 6.
    Minakami H, Hiramatsu Y, Koresawa M, et al. Guidelines for obstetrical practice in Japan: Japan Society of Obstetrics and Gynecology (JSOG) and Japan Association of Obstetricians and Gynecologists (JAOG) 2011 edition. J Obstet Gynaecol Res. 2011;37:1174–97.CrossRefPubMedGoogle Scholar
  7. 7.
    Ruvalcaba-Limon E, Cantu-de-Leon D, Leon-Rodriguez E, et al. The first Mexican consensus of endometrial cancer. Grupo de Investigacion en Cancer de Ovario y Tumores Ginecologicos de Mexico [in Spanish]. Rev Invest Clin. 2010;62:583, 85–605.Google Scholar
  8. 8.
    Korean Society of Gynecologic Oncology. Practice guideline for gynecologic cancer. In: Park SY (ed). Korean Society of Gynecologic Oncology; 2010.Google Scholar
  9. 9.
    Dowdy SC, Mariani A, Lurain JR. Uterine cancer. In: Berek JS (ed). Berek and Novak’s Gynecology. Philadelpia (PA): Lippincott Williams & Wilkins; 2012.Google Scholar
  10. 10.
    Stroup DF, Berlin JA, Morton SC, et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) Group. JAMA. 2000;283:2008–12.CrossRefPubMedGoogle Scholar
  11. 11.
    Fujiwara H, Saga Y, Takahashi K, et al. Omental metastases in clinical stage I endometrioid adenocarcinoma. Int J Gynecol Cancer. 2008;18:165–7.CrossRefPubMedGoogle Scholar
  12. 12.
    Dilek S, Dilek U, Dede M, Deveci MS, Yenen MC. The role of omentectomy and appendectomy during the surgical staging of clinical stage I endometrial cancer. Int J Gynecol Cancer. 2006;16:795–8.CrossRefPubMedGoogle Scholar
  13. 13.
    Metindir J, Dilek GB. The role of omentectomy during the surgical staging in patients with clinical stage I endometrioid adenocarcinoma. J Cancer Res Clin Oncol. 2008;134:1067–70.CrossRefPubMedGoogle Scholar
  14. 14.
    Chen SS, Spiegel G. Stage I endometrial carcinoma Role of omental biopsy and omentectomy. J Reprod Med. 1991;36:627–9.PubMedGoogle Scholar
  15. 15.
    Gehrig PA, Van Le L, Fowler WC Jr. The role of omentectomy during the surgical staging of uterine serous carcinoma. Int J Gynecol Cancer. 2003;13:212–5.CrossRefPubMedGoogle Scholar
  16. 16.
    Marino BD, Burke TW, Tornos C, et al. Staging laparotomy for endometrial carcinoma: assessment of peritoneal spread. Gynecol Oncol. 1995;56:34–8.CrossRefPubMedGoogle Scholar
  17. 17.
    Nieto JJ, Gornall R, Toms E, Clarkson S, Hogston P, Woolas RP. Influence of omental biopsy on adjuvant treatment field in clinical stage I endometrial carcinoma. BJOG. 2002;109:576–8.CrossRefPubMedGoogle Scholar
  18. 18.
    Saygili U, Kavaz S, Altunyurt S, Uslu T, Koyuncuoglu M, Erten O. Omentectomy, peritoneal biopsy and appendectomy in patients with clinical stage I endometrial carcinoma. Int J Gynecol Cancer. 2001;11:471–4.CrossRefPubMedGoogle Scholar
  19. 19.
    Zhang W, Bai P, Wu L. The clinical value of surgical-pathological staging for endometrial carcinoma [in Chinese]. Zhonghua Fu Chan Ke Za Zhi. 2001;36:479–82.PubMedGoogle Scholar
  20. 20.
    Ren YL, Wang HY, Shan BE, Ping B, Shi DR. Clinical implications of positive peritoneal cytology in endometrial cancer [in Chinese]. Zhonghua Fu Chan Ke Za Zhi. 2011;46:595–9.PubMedGoogle Scholar
  21. 21.
    Usubütün A, Ozseker HS, Himmetoglu C, Balci S, Ayhan A. Omentectomy for gynecologic cancer: how much sampling is adequate for microscopic examination? Arch Pathol Lab Med. 2007;131:1578–81.PubMedGoogle Scholar
  22. 22.
    Larson DM, Connor GP, Broste SK, Krawisz BR, Johnson KK. Prognostic significance of gross myometrial invasion with endometrial cancer. Obstet Gynecol. 1996;88:394–8.CrossRefPubMedGoogle Scholar
  23. 23.
    Lee TS, Kim JW, Kim SH, et al. Surgical practice patterns in endometrial cancer: results of the Korean Gynecologic Oncology Group survey. J Gynecol Oncol. 2009;20:107–12.PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
    Kong A, Johnson N, Kitchener HC, Lawrie TA. Adjuvant radiotherapy for stage I endometrial cancer. Cochrane Database Syst Rev. 2012;4:CD003916.PubMedCentralPubMedGoogle Scholar
  25. 25.
    Gynecologic Oncology Group. Pelvic radiation therapy or vaginal implant radiation therapy, paclitaxel, and carboplatin in treating patients with high-risk stage I or stage II endometrial cancer. Bethesda: National Cancer Institute; 2012.Google Scholar
  26. 26.
    Giuntoli RL 2nd, Gerardi MA, Yemelyanova AV, et al. Stage I noninvasive and minimally invasive uterine serous carcinoma: comprehensive staging associated with improved survival. Int J Gynecol Cancer. 2012;22:273–9.CrossRefPubMedGoogle Scholar
  27. 27.
    Oosterling SJ, van der Bij GJ, Bogels M, et al. Insufficient ability of omental milky spots to prevent peritoneal tumor outgrowth supports omentectomy in minimal residual disease. Cancer Immunol Immunother. 2006;55:1043–51.CrossRefPubMedGoogle Scholar

Copyright information

© Society of Surgical Oncology 2015

Authors and Affiliations

  • Won Duk Joo
    • 1
    • 2
  • Peter E. Schwartz
    • 1
  • Thomas J. Rutherford
    • 1
  • Seok Ju Seong
    • 2
  • Junbeom Ku
    • 3
  • Hyun Park
    • 2
  • Sang Geun Jung
    • 2
  • Min Chul Choi
    • 2
  • Chan Lee
    • 2
  1. 1.Department of Obstetrics, Gynecology and Reproductive SciencesYale University School of MedicineNew HavenUSA
  2. 2.Department of Obstetrics and GynecologyCHA University School of MedicineSeongnamRepublic of Korea
  3. 3.College of Literature, Science, and the ArtsUniversity of MichiganAnn ArborUSA

Personalised recommendations