Article:Sentinel lymph node mapping in endometrial cancer: a systematic review and meta-analysis. (5542296)

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This page is the ScienceSource HTML version of the scholarly article described at https://www.wikidata.org/wiki/Q38730345. Its title is Sentinel lymph node mapping in endometrial cancer: a systematic review and meta-analysis. and the publication date was 2017-07-11. The initial author is Hefeng Lin.

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Journal Information

Title: Oncotarget

Sentinel lymph node mapping in endometrial cancer: a systematic review and meta-analysis

  • Hefeng Lin
  • Zheyuan Ding
  • Vishnu Goutham Kota
  • Xiaoming Zhang
  • Jianwei Zhou

1 School of Medicine, Zhejiang University, Hangzhou 310058, China

2 Zhejiang Provincial Center for Disease Control and Prevention, Hangzhou 310051, China

3 Department of Gynecology, The Second Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou 310009, China

Publication date (collection): 7/2017

Publication date (epub): 3/2017

Abstract

Endometrial cancer is the most frequent tumor in the female reproductive system, while the sentinel lymph node (SLN) mapping for diagnostic efficacy of endometrial cancer is still controversial. This meta-analysis was conducted to evaluate the diagnostic value of SLN in the assessment of lymph nodal involvement in endometrial cancer. Forty-four studies including 2,236 cases were identified. The pooled overall detection rate was 83% (95% CI: 80–86%). The pooled sensitivity was 91% (95% CI: 87–95%). The bilateral pelvic node detection rate was 56% (95% CI: 48–64%). Use of indocyanine green (ICG) increased the overall detection rate to 93% (95% CI: 89–96%) and robotic-assisted surgery also increased the overall detection rate to 86% (95% CI: 79–93%). In summary, our meta-analysis provides strong evidence that sentinel node mapping is an accurate and feasible method that performs well diagnostically for the assessment of lymph nodal involvement in endometrial cancer. Cervical injection, robot-assisted surgery, as well as using ICG, optimized the sensitivity and detection rate of the technique. Sentinel lymph mapping may potentially leading to a greater utilization by gynecologic surgeons in the future.

Paper

INTRODUCTION

Endometrial cancer is the most frequently tumor of the female reproductive system in developed countries with an approximately 60,050 cases and 10,470 deaths for the year 2016 in the United States [[1]]. The surgical management of endometrial cancer is still controversial, especially in the early stage. The study shows that a complete lymphadenectomy may have no therapeutic benefit in patients with early-stage endometrial cancer [[2]]. Comprehensive lymphadenectomy not only increases operative time and blood loss but also is associated with surgical complications, such as blood vessel and nerve damage, lymphoedema, and lymphocyst formation [[3]]. The rate of long-term lymphedema directly attributed to lymphadenectomy was recently reported to be 23% [[4]]. Furthermore, lymphadenectomy imposes significant morbidity for the patients [[3]].

Lymph node status is a major prognostic factor and a criterion for adjuvant therapy in endometrial cancer. The concept of the sentinel lymph node (SLN), the node(s) most likely to harbor the first metastasis from the primary tumor, was first introduced in 1960 following observations associated with parotid gland carcinomas [[5]]. As the sentinel lymph node is relatively the first in a chain of lymph nodes, theoretically the sentinel node will be the first to encounter the effects of the metastatic form of the disease. If the sentinel node is negative, then it can be safely assumed that the remainder of the lymphatic basin is also unaffected by metastasis. The advantage of the distinctive benefits of SLN mapping is the opportunity to avoid “over-staging”, leading to a relatively lower morbidity than in the case of the performance of a full lymphadenectomy and the potential for improved diagnostic accuracy [[6]]. As a surgical technique, the SLN mapping has been implemented in the standard of treatment for patients with melanoma and breast cancer [[7]].

If the SLN concept is valid in endometrial cancer, most patients, especially women affected with endometrial cancer in the early stage could avoid the risks associated with the lymphadenectomy. However, the diagnostic efficacy of SLN mapping in endometrial cancer is still controversial. Therefore, we performed a meta-analysis to evaluate different sentinel lymph node mapping techniques and their corresponding detection rates and sensitivity in endometrial cancer.

RESULTS

Overall, 2,205 studies were retrieved through the electronic databases searching. Among these, 859 (39.0%) studies were removed as duplicates. After title and abstract evaluation, 233 (10.6%) remained for full review. Of these, 189 (8.6%) full-text articles were additionally excluded for the following reasons: 8 (0.36%) had low sample size(fewer than 7 patients); 56 (2.5%) not concerned with endometrial cancer; 62 (2.8%) not mainly focused on SLN mapping; 12 (0.54%) without histological or immunohistological results; 6 (0.27%) reported only the numbers of metastasized lymph nodes but not the number of patients; 6 (0.27%) from the same research team using the same database; 10 (0.45%) were animal studies; 3 (0.1%) were case reports; 7 (0.32%) were letters; 19 (0.86%) were reviews. Thus, 44 (2.0%) studies [[11][54]] were deemed as eligible by the authors (involving 2,236 patients) after conducting a comprehensive and through literature search. Figure 1 shows the process involved in the assessment of the studies and in accordance to the process highlighted in the figure the studies were identified, those of them that fulfilled the conditions detailed earlier were included and those that didn't were excluded.

Figure 1

Flow diagram of studies identified, included, and excluded

Sensitivity

The pooled sensitivity for all studies deemed eligible (n = 44) by the authors was 91% (95% CI: 87–95%), the Cochran Q value was 49.90 (p = 0.22 and I2 = 13.82%). The forest plot of sensitivity pooling is shown in Figure 2.

Figure 2

Forest plot of pooled sensitivity and 95% CI in SLN mapping in endometrial cancer

The funnel plot of the sensitivity pooling and the funnel plot of the sensitivity pooling by using trim and fill method are shown in Figure 3. The egger's regression intercept was found out to be 2.34 (p = 0.031).

Figure 3

(A) Funnel plot of pooled sensitivity. (B) Funnel plot of pooled sensitivity by using trim and fill method.

Overall SLN detection rate

Figure 4 shows the forest plot associated with the overall SLN detection rate. The pooled detection rate was 83 % (95% CI: 80–86%), with heterogeneity I2 = 78.9% (p = 0.000).

Figure 4

Forest plot of pooled overall detection rate and 95% CI in SLN mapping in endometrial cancer

The funnel plot of the overall SLN detection rate pooling and the funnel plot of the overall SLN detection rate pooling are shown in Figure 5. The egger's regression intercept was −7.06 (p = 0.000).

Figure 5

(A) Funnel plot of pooled overall SLN detection rate. (B) Funnel plot of pooled overall SLN detection rate by using trim and fill method.

Bilateral SLN detection rate

Figure 6 shows the forest plot of the bilateral SLN detection rate. The bilateral SLN detection rate was observed to be 56% (95% CI: 48–63%), with heterogeneity I2 = 91.4% (p = 0.000).

Figure 6

Forest plot of pooled bilateral SLN detection rate and 95%CI in SLN mapping in endometrial cancer

Sub-group analysis

The sentinel lymph node detection rate and sensitivity were related to the mapping method employed (blue dye alone, radiotracer dye with blue dye, ICG), the surgical approach followed (laparotomy, laparoscopy, robotic assistance) and the site of dye injection (cervical injection, uterine injection) (Table 1). Use of ICG showed high pooled overall detection rate: 93% (95% CI: 89–96%) and high pooled bilateral detection rate: 78% (95% CI: 72–84%). The Robot-assisted surgery also had high pooled overall detection rate: 86% (95% CI: 79–93%) and pooled bilateral detection rate: 62% (95%CI: 43–80%). The sensitivity and overall detection rate were high in patients in whom cervical injection was the site of dye injection 93% (95% CI: 87–96%) and 86% (95% CI: 83–89%), respectively and both blue dye and radiotracer dye were used for mapping 92% (95% CI: 84–96%) and 86% (95% CI: 82–90%), respectively. Laparoscopic surgery showed higher pooled sensitivities 96 % (95% CI: 88–99%).

Table 1

Results of sub-group analysis

Sub-group Detection rate (95% CI) Sensitivity (95% CI) Bilateral detection rate (95% CI)
Surgical approach Laparoscopy 82% (78–87%) 96% (88–99%) 58% (47–69%)
Laparotomy 77% (71–84%) 89% (80–95%) 47% (32–61%)
Robotic assistance 86% (79–93%) 90% (77–96%) 62% (43–80%)
Mapping method Blue dye 76% (71–81%) 90% (79–96%) 44% (38–50%)
ICG 93% (89–96%) 87% (76–93%) 78% (72–84%)
Tc-99m+blue dye 86% (82–90%) 92% (84–96%) 56% (41–71%)
Injection site Cervical injection 86% (83–89%) 93% (87–96%) 60% (52–69%)
Uterine injection 76% (68–83%) 88% (78–93%) 47% (11–84%)

Abbreviations: ICG, indocyanine green; Tc-99m, technecium-99.

DISCUSSION

To our knowledge, this is the newest meta-analysis focused on the diagnostic efficacy of sentinel lymph node mapping in endometrial cancer. In our meta-analysis of 44 studies comprising 2,236 cases, sentinel node mapping yielded a pooled detection rate of 83%. The pooled sensitivity implies that 91% of occult lymph node metastases could be diagnosed by SLN mapping, which seems to be equivalent to those achieved in patients with breast cancer (sensitivity 91%) [[55]]. However, bilateral nodes were detected in only 59% (26 studies) of the patients. The Endometrium as a midline organ and it exhibits two different pathways of lymphatic drainage: right and left [[28]]. The bilateral detection method has been used for other midline organs such as the penis with fairly promising results [[56]]. In the present study,the rate of bilateral SLN detection was between 89% (in the study conducted by Martinelli et al.) [[51]] and 19% (in the study conducted by Torné et al.) [[34]], and the pooled bilateral detection rate was 56% (95% CI: 48–64%). Therefore, achieving high bilateral SLN detection rates of endometrial cancer is mandatory to implement the SLN mapping as a routine component of clinical practice.

It should be mentioned that in the previous meta-analyses focusing on the diagnostic efficacy of SLN mapping in endometrial cancer, Kang et al. [[57]] reported a pooled detection rate of 78% (95% CI: 73–84%) (n = 1,101), while Ansari et al. [[58]] reported a pooled detection rate and sensitivity of 77.8% (95% CI: 74–82%) and 89% (95% CI: 83–93%) respectively (n = 2,071). Compared to these previous meta-analyses, our research found higher detection rate of 83% (95% CI: 80–86%) (n = 2,236) and sensitivity of 91% (95% CI: 87–95%). Since previous two meta-analyses were published several years ago, our meta-analysis included the newest results of the recent studies, which makes it more valid.

In addition, the studies included in our systematic review were heterogeneous and therefore gave rise to the need for conducting a sub-group analysis to explore the reasons for the observed heterogeneity. Laparoscopic surgery and robot-assisted surgery, were associated with high detection rates and sensitivities when compared with an open surgery based approach. The pilot study conducted by Mais et al. [[26]] showed that the high detection rates obtainable through laparoscopy were not reproducible through laparotomy. The different detection rates observed through laparoscopy or through laparotomy might depend on the different time intervals elapsing between the injection of the vital dye into the cervix and the surgical SLN assessment in the pelvic basin. In fact, this time interval was always found to be shorter in the case of laparoscopy than for laparotomy. The current study also showed that the pooled sensitivity and detection rates in endometrial cancer patients are high for SLN mapping when the mapping was carried out using ICG. When the mapping was carried out using solely the blue dye, the pooled detection rate was observed to be rather low. Moreover, there are some disadvantages of the use of the blue dye. Allergic reactions to the blue dye were observed in 0.14–3% of the patients, including urticaria, skin rashes, erythema, blue hives, cardiovascular collapse, and anaphylactic shock. Other side effects include temporary skin tattooing, blue discoloration of the operative field following peritumoral injection, blue-colored urine for up to 24 hrs. following administration, and a factitious drop in intraoperative oxygen saturation measured by pulse oximetry. Furthermore, the teratogenicity and the long-term toxicity associated with the blue dye are unknown and could have serious effects on pregnancy [[59], [60]]. Indocyanine green (ICG) represents a feasible alternative to the more traditional methods of sentinel lymph node (SLN) mapping, and the interest associated with this promising tracer is growing. A recent meta-analysis conducted by Ruscito et al. [[61]] demonstrated that ICG SLN mapping seems to be equivalent to the combination of blue dyes and Tc-99m in terms of overall and bilateral detection rates in uterine malignancies. The good toxicity profile and ease of use of ICG, which does not require the injection to be administered in a controlled environment is also very desirable. Another issue in SLN mapping pertains to the identification of the optimal injection site for the radiocolloid /dye in patients with endometrial cancer. A comprehensive sub-group analysis showed that the use of cervical injection as the dye injection approach was found to cause an increase of 10% and 5% in the detection rate and sensitivity respectively, as compared to the use of uterine injection as the dye injection approach. It seems to be a lack of sufficient consensus about the best site of injection. The cervical injection approach is a method which is easy to carry out, reproducible, and is very suitable for standardization.

The meta-analysis performed during the course of this study has the following limitations that must be taken into account. First, the results presented in the current study were based on unadjusted estimates; more accurate outcomes would result from the adjustments made to be considered for other confounders such as age, body mass index, cancer stage, and so on. Second, the studies included in this analysis were not sufficient enough, especially from the perspective of a subgroup analysis. Thus, a potential publication bias is very likely to be associated with the results provided in this study in spite of evidence obtained from the statistical tests performed. Finally, only English and Chinese reports have been included in the analysis and consequently this might lead to the study not considering the data from other relevant studies published in other languages, which may result in causing a potential language bias.

In conclusion, the present results confirmed that sentinel lymph node mapping is a feasible and reliable approach that performs well diagnostically for the assessment of lymph nodal involvement in endometrial cancer. We also found that SLN mapping using some new techniques, such as ICG and robot-assisted surgery demonstrated higher detection rates compared to other modalities. The use of cervical injection and the mode of dye injection for both the blue dye and the radiotracer of the mapping material can optimize the sensitivity and detection rate of the technique. Further clinical trials are required to investigate the relationship between lymphadenectomy guided by SLN mapping and prognosis of endometrial cancer in the future.

MATERIALS AND METHODS

Search strategy

A comprehensive literature search on the retrieved publications (the last search was done in November, 2016) was performed independently by two authors associated with this current study. The language of studies was limited to English and Chinese only. The primary sources for the literature search were the electronic databases: Pubmed, Embase, Medline and the Cochrane Library. The predefined keywords used for the search were “sentinel lymph node” and “endometrial cancer”. A search algorithm that selected and screened results based on a combination with the following search terms: “sentinel AND (endometri* OR uterus OR uterine OR corpus uteri ) AND (cancer OR neoplasm* OR carcinoma* OR malignanc* OR tumo*)” was used to perform the literature search detailed in this study.

Inclusion and exclusion criteria

For evaluating the diagnostic performance of sentinel lymph node mapping in endometrial cancers, the studies in accordance to the following inclusion criteria were included: (1) Studies with the enrollment of at least 7 women diagnosed with endometrial cancer; (2) The SLN mapping was the study's primary focus; (3) Studies validated by pelvic with/without para-aortic lymph node dissection and pathological examination including H&E (hematoxylin-eosin) staining or immunohistochemistry (IHC) were taken as the reference standard; (4) SLN mapping as the diagnostic method; (5) Studies where the total number of enrolled patients as well as those with detected SLN were both reported; (6) Studies that reported the total number of patients with a positive lymph node diagnosis, as well as those with false negative results.

Review articles, letters, comments, conference proceedings, unpublished data and case-reports were excluded. To avoid overlapping patient data in duplicate publications, we included the more recent articles with the largest sample sizes.

Study quality assessment

The quality assessment of studies included in this article was undertaken by authors Lin and Zhang. The “QUADAS-2” (Quality Assessment of Diagnostic Accuracy Studies-2) tool, an official tool for assessing the quality of the diagnosis accuracy of a study (launched in 2011) was used to assist with the above-mentioned quality assessment [[8]]. The core “QUADAS-2” items used in our study are detailed outlined in the Appendix Table 1. “QUADAS-2” divided the assessment items into the risk of bias and the applicability, and has several items including: patient selection, index test, reference standard, flow and timing. The criteria could be scored as “yes”,”no”, or “not reported” in the publication.

Data abstraction

Data from the included studies were extracted and summarized independently by the two authors mentioned earlier (Lin and Zhang). The extracted data primarily included (Supplementary Table 1): first author, publication year, country, sample size of the study, detection rate, tracer, injection site, pathology assessment and surgical approach. Wherever possible, the SLN detection rate was calculated in patients with bilateral sentinel node identification. The sensitivity associated with the sentinel lymph node procedure was defined as the total number of true positives in patients with a positive histopathology. A positive sentinel node was considered as true positive (TP) irrespective to the status of the other nodes, and a true negative (TN) was a negative sentinel node only if all other non-sentinel nodes were negative. A false negative (FN) was defined as positive non-SLN with negative SLN. The SLN detection rate can be defined as the percentage of patients in which at least one SLN was identified.

Statistical analysis

The statistical analysis tool, Stata 12.0 software (StataCorp, College Station, Texas, USA) was employed to perform the aggregate data meta-analyses and evaluate the heterogeneity of the included studies. The random effects model was applied for calculating the overall detection rate, the bilateral detection rate, and the sensitivity from the data provided in the source articles. The results were depicted graphically as forest plots. The pooled data was presented with 95% confidence intervals (95% CI). The potential heterogeneity of the sensitivity and the detection rate was analyzed with the Cochrane Q test (the p-values less than 0.05 were considered as statistically significant). I2 index was used to quantify the heterogeneity, analyzing how much of the variance associated with the included studies was real and wasn't due to sampling errors. Funnel plots, Egger's regression intercepts [[9]], and the Duval and Tweedie's [[10]] “trim and fill” method were used for the evaluation of publication bias. A subgroup analysis was performed for expolring the heterogeneity in three variables: surgical approach, mapping method, injection site.

SUPPLEMENTARY TABLE AND APPENDIX TABLE

Acknowledgements

ACKNOWLEDGMENTS AND FUNDING

The study is supported by the National Natural Science Foundation of China, Grant No. 81371881 and The Natural Science Foundation of Zhejiang Province, China Grant No. LY12H16012.

References

  1. RL SiegelKD MillerA JemalCancer statistics, 2016CA Cancer J Clin20166673010.3322/caac.2133226742998
  2. K MayA BryantHO DickinsonS KehoeJ MorrisonLymphadenectomy for the management of endometrial cancerCochrane Database Syst Rev2010651399140010.1002/14651858.CD007585.pub2
  3. SC DowdyBJ BorahJN Bakkum-GamezAL WeaverME McGreeLR HaasGL KeeneyA MarianiKC PodratzProspective assessment of survival, morbidity, and cost associated with lymphadenectomy in low-risk endometrial cancerGynecol Oncol201212751010.1016/j.ygyno.2012.06.03522771890
  4. KJ YostAL ChevilleMM Al-HilliA MarianiBA BarretteME McGreeAL WeaverSC DowdyLymphedema after surgery for endometrial cancer: prevalence, risk factors, and quality of lifeObstet Gynecol20141243071510.1097/AOG.000000000000037225004343
  5. EA GouldT WinshipPH PhilbinHH KerrObservations on a “sentinel node” in cancer of the parotidCancer19601377810.1002/1097-0142(196001/02)13:1<77::AID-CNCR2820130114>3.0.CO;2-D13828575
  6. J EmersonK RobisonEvaluation of sentinel lymph nodes in vulvar, endometrial and cervical cancersWorld J Obstet Gynecol20165788610.5317/WJOG.v5.i1.78
  7. RM CabanasAn approach for the treatment of penile carcinomaCancer19773945646610.1002/1097-0142(197702)39:2<456::AID-CNCR2820390214>3.0.CO;2-I837331
  8. PF WhitingAW RutjesME WestwoodS MallettJJ DeeksJB ReitsmaMM LeeflangJA SternePM BossuytQUADAS-2 GroupQUADAS-2: a revised tool for the quality assessment of diagnostic accuracy studiesAnn Intern Med20111555293610.7326/0003-4819-155-8-201110180-0000922007046
  9. M EggerG Davey SmithM SchneiderC MinderBias in meta-analysis detected by a simple, graphical testBMJ19973156293410.1136/bmj.315.7109.6299310563
  10. S DuvalR TweedieTrim and fill: A simple funnel-plot-based method of testing and adjusting for publication bias in meta-analysisBiometrics2000564556310.1111/j.0006-341X.2000.00455.x10877304
  11. TW BurkeC LevenbackC TornosM MorrisJT WhartonDM GershensonIntraabdominal lymphatic mapping to direct selective pelvic and paraaortic lymphadenectomy in women with high-risk endometrial cancer: results of a pilot studyGynecol Oncol1996621697310.1006/gyno.1996.02118751545
  12. E PelosiV ArenaB BaudinoM BellòM GiustiT GargiuloD PalladinG BisiPreoperative lymphatic mapping and intraoperative sentinel lymph node detection in early stage endometrial cancerNucl Med Commun200324971510.1097/00006231-200309000-0000512960596
  13. Z HolubA JaborJ LukacL KlimentLaparoscopic detection of sentinel lymph nodes using blue dye in women with cervical and endometrial cancerMed Sci Monit200410CR5879115448599
  14. L LelievreS CamatteMA Le Frere-beldaK KerrouM FroissartR TaurelleF VildeF LecuruSentinel lymph node biopsy in cervix and corpus uteri cancersInt J Gynecol Cancer200414271810.1111/j.1048-891X.2004.014210.x15086726
  15. H NiikuraC OkamuraH UtsunomiyaK YoshinagaJ AkahiraK ItoN YaegashiSentinel lymph node detection in patients with endometrial cancerGynecol Oncol2004926697410.1016/j.ygyno.2003.10.03914766264
  16. A BastaK PityńskiP BastaA Hubalewska-HołaM OpławskiD PrzeszlakowskiSentinel node in gynaecological oncologyRep Pract Oncol Radiother200510242710.1016/S1507-136771114-7
  17. LT GienJS KwonMS CareySentinel node mapping with isosulfan blue dye in endometrial cancerJ Obstet Gynaecol Can20052711071210.1016/S1701-216330393-016524529
  18. M MaccauroG LucignaniG AlibertiC VillanoMR CastellaniE SolimaE BombardieriSentinel lymph node detection following the hysteroscopic peritumoural injection of 99mTc-labelled albumin nanocolloid in endometrial cancerEur J Nucl Med Mol Imaging2005325697410.1007/s00259-004-1709-415625604
  19. C AltgassenJ PagenstecherD HornungK DiedrichA HornemannA new approach to label sentinel nodes in endometrial cancerGynecol Oncol20071054576110.1016/j.ygyno.2007.01.02117313975
  20. JF DelaloyeS PampallonaE ChardonnensM FicheHA LehrP De GrandiAB DelaloyeIntraoperative lymphatic mapping and sentinel node biopsy using hysteroscopy in patients with endometrial cancerGynecol Oncol2007106899310.1016/j.ygyno.2007.03.00317442383
  21. LA LopesSM NicolauFF BaracatEC BaracatWJ GonçalvesHV SantosRG LopesUG LippiSentinel lymph node in endometrial cancerInt J Gynecol Cancer2007171113710.1111/j.1525-1438.2007.00909.x17386045
  22. X YanG LiL ChenG WangH ShangT LinY HanJ GuanA pilot study on sentinel lymph nodes identification in patients with cervical cancer or endometrial cancerPract Obstet Gynecol2007237373910.3969/j.issn.1003-6946.2007.12.014
  23. M BallesterG DubernardR RouzierE BarrangerE DaraiUse of the sentinel node procedure to stage endometrial cancerAnn Surg Oncol2008151523910.1245/s10434-008-9841-118322758
  24. AS BatsD ClémentF LarousserieMA Le Frère-BeldaN Pierquet-GhazzarC HignetteF LécuruDoes sentinel node biopsy improve the management of endometrial cancer? Data from 43 patientsJ Surg Oncol200897141510.1002/jso.2085718050286
  25. B LiL WuX LiH LuP BaiS LiW ZhangJ GaoSentinel lymph node identification in endometrial cancerClin Oncol Cancer Res20096124810.1007/s11805-009-0124-9
  26. V MaisM PeirettiT GargiuloG ParodoMG CirronisGB MelisIntraoperative sentinel lymph node detection by vital dye through laparoscopy or laparotomy in early endometrial cancerJ Surg Oncol20101014081210.1002/jso.2149620119976
  27. J QuY QiW LiThe preliminary research of sentinel lymph node enhancement identification detection in endometrial cancerJ Jining Med Univ20103339840010.3969/j.issn.1000-9760.2010.06.008
  28. M BallesterG DubernardF LécuruD HeitzP MathevetH MarretD QuerleuF GolfierE LeblancR RouzierE DaraïDetection rate and diagnostic accuracy of sentinel-node biopsy in early stage endometrial cancer: a prospective multicentre study (SENTI-ENDO)Lancet Oncol2011124697610.1016/S1470-204570070-521489874
  29. RW HollowayRA BravoJA RakowskiJA JamesCN JeppsonSB IngersollS AhmadDetection of sentinel lymph nodes in patients with endometrial cancer undergoing robotic-assisted staging: a comparison of colorimetric and fluorescence imagingGynecol Oncol201212625910.1016/j.ygyno.2012.04.00922507531
  30. EC RossiA IvanovaJF BoggessRobotically assisted fluorescence-guided lymph node mapping with ICG for gynecologic malignancies: a feasibility studyGynecol Oncol2012124788210.1016/j.ygyno.2011.09.02521996262
  31. E SolimaF MartinelliA DittoM MaccauroM CarcangiuL MarianiS KusamuraR FontanelliB GrijuelaF RaspagliesiDiagnostic accuracy of sentinel node in endometrial cancer by using hysteroscopic injection of radiolabeled tracerGynecol Oncol20121264192310.1016/j.ygyno.2012.05.02522659192
  32. M BallesterI NaouraE ChéreauJ SerorAS BatsA BricouE DaraïSentinel node biopsy upstages patients with presumed low- and intermediate-risk endometrial cancer: results of a multicenter studyAnn Surg Oncol2013204071210.1245/s10434-012-2683-x23054119
  33. BJ MosgaardVR SkovlundHW HendelPromising results using sentinel node biopsy as a substitute for radical lymphadenectomy in endometrial cancer stagingDan Med J201360A466523809974
  34. A TornéJ PahisaS Vidal-SicartS Martínez-RomanP ParedesB PuertoS AlbelaP FustéA PerisinottiJ OrdiTransvaginal ultrasound-guided myometrial injection of radiotracer (TUMIR): a new method for sentinel lymph node detection in endometrial cancerGynecol Oncol2013128889410.1016/j.ygyno.2012.10.00823085461
  35. F VidalP LeguevaqueS MottonJ DelotteG FerronD QuerleuA RafiiEvaluation of the sentinel lymph node algorithm with blue dye labeling for early-stage endometrial cancer in a multicentric settingInt J Gynecol Cancer20132312374310.1097/IGC.0b013e31829b1b9823839245
  36. PH DesaiP HughesDH TobiasN TchaboPB HellerC DiseBM SlomovitzAccuracy of robotic sentinel lymph node detection (RSLND) for patients with endometrial cancer (EC)Gynecol Oncol201413519620010.1016/j.ygyno.2014.08.03225175452
  37. S KadkhodayanZ ShiravaniM HasanzadehN SharifiZ YousefiA FattahiR SadeghiLymphatic mapping and sentinel node biopsy in endometrial cancer—a feasibility study using cervical injection of radiotracer and blue dyeNucl Med Rev Cent East Eur20141755810.5603/NMR.2014.001725088102
  38. C López-De la Manzanara CanoJM Cordero GarcíaC Martín-FranciscoJ Pascual-RamírezCP ParraC Céspedes CasasSentinel lymph node detection using 99mTc combined with methylene blue cervical injection for endometrial cancer surgical management: a prospective studyInt J Gynecol Cancer20142410485310.1097/IGC.000000000000015824927249
  39. J MückeR KlapdorM SchneiderF LängerKF GratzP HillemannsH HertelIsthmocervical labelling and SPECT/CT for optimized sentinel detection in endometrial cancer: technique, experience and resultsGynecol Oncol20141342879210.1016/j.ygyno.2014.05.00124823647
  40. E RaimondM BallesterD HudryS BendifallahE DaraïO GraesslinC CoutantImpact of sentinel lymph node biopsy on the therapeutic management of early-stage endometrial cancer: Results of a retrospective multicenter studyGynecol Oncol20141335061110.1016/j.ygyno.2014.03.01924642092
  41. T AllamehV HashemiF MohammadizadehF BehnamfarSentinel lymph node mapping in early stage of endometrial and cervical cancersJ Res Med Sci2015201697325983771
  42. R EitanG SabahH KrissiO RabanA Ben-HaroushC GoldschmitH LevaviY PeledRobotic blue-dye sentinel lymph node detection for endometrial cancer - Factors predicting successful mappingEur J Surg Oncol20154116596310.1016/j.ejso.2015.09.00626433709
  43. MM FarghaliIS AllamIA AbdelazimOS El-KadyAR RashedWY GareerMS SweedAccuracy of Sentinel Node in Detecting Lymph Node Metastasis in Primary Endometrial CarcinomaAsian Pac J Cancer Prev2015166691610.7314/APJCP.2015.16.15.669126434896
  44. J HowWH GotliebJZ PressJ AbitbolM PelmusA FerenczyS ProbstR GotliebS BrinS LauComparing indocyanine green, technetium, and blue dye for sentinel lymph node mapping in endometrial cancerGynecol Oncol20151374364210.1016/j.ygyno.2015.04.00425870917
  45. A RajanbabuV MuraliYS NatarajDK VijaykumarDetection of Sentinel Lymph Nodes in Endometrial Cancer with Intracervical Indocyanine Green Injection and Robotically Assisted Near Infrared Imaging: A Feasibility Study in Indian SettingIndian Journal of Gynecologic Oncology2015131610.1007/s40944-015-0020-6
  46. O TouhamiXB TrinhJ GregoireA SebastianelliMC RenaudK GrondinM PlanteIs a More Comprehensive Surgery Necessary in Patients With Uterine Serous Carcinoma?Int J Gynecol Cancer20152512667010.1097/IGC.000000000000048826067862
  47. A BudaC CrivellaroF EliseiG Di MartinoL GuerraE De PontiM CuzzocreaD GiulianiF SinaS MagniC LandoniR MilaniImpact of Indocyanine Green for Sentinel Lymph Node Mapping in Early Stage Endometrial and Cervical Cancer: Comparison with Conventional Radiotracer (99m)Tc and/or Blue DyeAnn Surg Oncol20162321839110.1245/s10434-015-5022-126714944
  48. J EhrismanAA SecordA BerchuckPS LeeN Di SantoM Lopez-AcevedoG BroadwaterFA ValeaLJ HavrileskyPerformance of sentinel lymph node biopsy in high-risk endometrial cancerGynecol Oncol Rep201617697110.1016/j.gore.2016.04.00227453926
  49. F EliseiC CrivellaroD GiulianiC DolciE De PontiL MontanelliM La MannaL GuerraM ArosioC LandoniA BudaSentinel-node mapping in endometrial cancer patients: comparing SPECT/CT, gamma-probe and dyeAnn Nucl Med201731939910.1007/s12149-016-1137-027815812
  50. A MarkusAS RayD BollaJ MüllerPA DienerT WendlerR HornungSentinel lymph node biopsy in endometrial and cervical cancers using freehand SPECT—first experiencesGynecol Surg20161810.1007/s10397-016-0969-x26918000
  51. F MartinelliA DittoG BoganiM SignorelliV ChiappaD LorussoF RaspagliesiLaparoscopic sentinel node mapping in endometrial cancer following hysteroscopic injection of indocyanine greenJ Minim Invasive Gynecol201623S99S10010.1016/j.jmig.2016.08.244
  52. PJ PaleyDS VeljovichJZ PressC IsacsonE PizerC ShahA prospective investigation of fluorescence imaging to detect sentinel lymph nodes at robotic-assisted endometrial cancer stagingAm J Obstet Gynecol2016215117.e1710.1016/j.ajog.2015.12.04626743505
  53. A PapadiaS ImbodenF SiegenthalerML GasparriS MohrS LanzMD MuellerLaparoscopic Indocyanine Green Sentinel Lymph Node Mapping in Endometrial CancerAnn Surg Oncol20162322061110.1245/s10434-016-5090-x26790667
  54. MB SchiavoneO ZivanovicQ ZhouMM Leitao JrDA LevineRA SoslowKM AlektiarV MakkerA IasonosNR Abu-RustumSurvival of Patients with Uterine Carcinosarcoma Undergoing Sentinel Lymph Node MappingAnn Surg Oncol20162319620210.1245/s10434-015-4612-225994210
  55. U VeronesiG PaganelliG VialeA LuiniS ZurridaV GalimbertiM IntraP VeronesiC RobertsonP MaisonneuveG RenneC De CiccoF De LuciaA randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancerN Engl J Med20033495465310.1056/NEJMoa01278212904519
  56. R SadeghiH GholamiSR ZakaviVR KakhkiKT TabasiS HorenblasAccuracy of sentinel lymph node biopsy for inguinal lymph node staging of penile squamous cell carcinoma: systematic review and meta-analysis of the literatureJ Urol2012187253110.1016/j.juro.2011.09.05822088350
  57. S KangHJ YooJH HwangMC LimSS SeoSY ParkSentinel lymph node biopsy in endometrial cancer: meta-analysis of 26 studiesGynecol Oncol2011123522710.1016/j.ygyno.2011.08.03421945553
  58. M AnsariMA RadM HassanzadehH GholamiZ YousefiVR DabbaghR SadeghiSentinel node biopsy in endometrial cancer: systematic review and meta-analysis of the literatureEur J Gynaecol Oncol20133438740124475571
  59. AM ArgonU DuygunE AcarG DagliozL YenjayO ZekiogluM KapkacThe use of periareolar intradermal Tc-99m tin colloid and peritumoral intraparenchymal isosulfan blue dye injections for determination of the sentinel lymph nodeClin Nucl Med20063179580010.1097/01.rlu.0000246855.80027.b717117076
  60. SP BagariaMB FariesDL MortonSentinel node biopsy in melanoma: Technical considerations of the procedure as performed at the john wayne cancer instituteJ Surg Oncol201010166967610.1002/jso.2158120512942
  61. I RuscitoML GasparriEI BraicuF BellatiL RaioJ SehouliMD MuellerPB PaniciA PapadiaSentinel Node Mapping in Cervical and Endometrial Cancer: Indocyanine Green Versus Other Conventional Dyes-A Meta-AnalysisAnn Surg Oncol20162337495610.1245/s10434-016-5236-x27160526
The underlying source XML for this text is taken from https://www.ebi.ac.uk/europepmc/webservices/rest/PMC5542296/fullTextXML. The license for the article is Creative Commons Attribution 3.0 Unported. The main subject has been identified as endometrial carcinoma.