Extraperitoneal Laparoscopy for Para-Aortic Lymphadenectomy in Endometrial Carcinoma Staging: An Approach with Higher Efficiency

doi:10.21203/rs.3.rs-402131/v1

Download PDF

Research Article

Extraperitoneal Laparoscopy for Para-Aortic Lymphadenectomy in Endometrial Carcinoma Staging: An Approach with Higher Efficiency

https://doi.org/10.21203/rs.3.rs-402131/v1

This work is licensed under a CC BY 4.0 License

You are reading this latest preprint version

Background: To compare the surgical outcomes of extraperitoneal laparoscopic, transperitoneal laparoscopic, and laparotomic para-aortic lymphadenectomy in endometrial carcinoma staging.

Methods: We retrospectively reviewed data of all patients diagnosed with primary endometrial carcinoma who were treated at the Department of Gynecologic Oncology, Fudan University Shanghai Cancer Center from 1 January 2017 to 31 December 2019. The numbers of para-aortic lymph nodes, surgical time, complications, blood loss and hospital stay were compared. The patients' medical records and pathological reports were carefully reviewed. Statistical significance was defined as p< 0.05.

Results: We retrospectively compared patients who underwent extraperitoneal laparoscopy (Group E, n=20), transperitoneal laparoscopy (Group T, n=21), and laparotomy (Group L, n=135). The median number of para-aortic lymph nodes was significantly higher in Group E than in Group T andL (9.5, 5, and 6, respectively; p=0.004 and 0.0004, respectively). All patients in Group E underwent successfully dissction to the renal vessel level. The median operation time was significantly shorter in Group L than in Groups T and E (94, 174, and 233 minutes, respectively; p<0.0001). The median estimated blood loss volume was higher in Group L than in Groups T and E (200, 100, and 142.5 ml, respectively; all comparisons p<0.001), and the length of hospital stay was significantly longer in Group L than in Groups T and E (6, 56, and 6 days, respectively; all comparisons p<0.001).

Conclusion: The extraperitoneal laparoscopic approach for staging endometrial carcinoma harvested higher numbers of para-aortic lymph nodes which could be considered for endometrial carcinoma staging, especially for para-aortic lymph node harvest.

Surgery

Oncology

endometrial carcinoma

extraperitoneal

transperitoneal

laparotomy

minimally invasive

Transperitoneal laparoscopic lymphadenectomy was first reported in the early 1990s for surgical staging [1]. As confirmed by the Gynecologic Oncology Group (GOG), the transperitoneal laparoscopic approach is a satisfactory method for surgical staging of endometrial carcinoma[2]. The extraperitoneal approach was first reported in 1995 and was primarily used to evaluate para-aortic metastases in patients with cervical cancer [1, 3, 4]; more attention has been given to staging of patients with endometrial cancer via this approach in recent years[5, 6]. Although laparoscopic surgery is the preferred approach for endometrial cancer, with less blood loss and a shorter length of hospital stay[7], minimally invasive approaches were reportedly used by only 60% of the gynecological oncologists[8].

Computed tomography, magnetic resonance imaging (MRI) and positron-emission tomography (PET-CT) were used for evaluation of lymph node status. The sensitivity of computed tomography in detection of paraaortic lymph node metastases were 34%[9]. Sensitivity of MRI vs PET-CT[10] were 57% and 75%, respectively [9]. For PET-CT with specificity of 92.7%[10]. For women with a completely negative PET scan, 12% had disease spread to nodes along the aorta[11]. According to these results, surgical evaluation of lymph node status is necessary. However, 50% of the surgeons routinely stopped at the inferior mesenteric artery if lymphadenectomy was needed, and only 11% reported routinely dissecting nodes to the level of the renal vessels(RVs)[8]. Because 77% of patients with endometrial carcinoma with positive para-aortic lymph nodes have metastases above the inferior mesenteric artery [7], and because as many as 10% of patients with clinically early endometrial carcinoma have infrarenal node involvement[12], the upper limit for para-aortic lymphadenectomy must be the left RV. Removing more inframesenteric nodes significantly increases the likelihood of finding cancer metastasis for endometrial cancer[13], and dissecting the infrarenal nodes during staging can add a 10% survival advantage[14].

The left aortic nodes contain 63% of all aortic nodes, which makes the left-sided extraperitoneal technique much easier and suitable for lymph node dissection in patients with endometrial cancer[15, 16]. With its lower risk of intestinal and urinary injury and adhesions, the extraperitoneal technique is considered superior to the transperitoneal approach in both obese and nonobese patients[17]. One study showed that in nonobese patients, the transperitoneal approach was associated with a higher number of harvested lymph nodes[17].

To date, comparisons between transperitoneal or extraperitoneal laparoscopic or robotic transperitoneal para-aortic lymphadenectomy approaches were performed primarily in gynecological oncology[7, 18, 19], few study focused on a systemic study of the surgical procedure in endometrial carcinoma staging. Our aim was to compare the surgical outcomes including numbers of para-aortic lymph nodes, surgical time, intra- and post-operative complications, blood loss and hospital stay of systemic staging of endometrial carcinoma via extraperitoneal, transperitoneal laparoscopic and laparotomic approaches.

Patients and inclusion criteria

We retrospectively collected and reviewed data for all patients diagnosed with primary endometrial carcinoma who were treated at the Department of Gynecologic Oncology, Fudan University Shanghai Cancer Center from 1 January 2017 to 31 December 2019.This study was conducted until 1 April, 2020. We included data for patients who underwent systemic staging, including para-aortic lymphadenectomy, and excluded patients who did not undergo para-aortic lymphadenectomy. Patients with a synchronous primary ovarian tumor were also excluded. Clinical information, physical examination notes, operation records, and pathology records were carefully reviewed. Tumor stage was classified according to the 2009 International Federation of Gynecology and Obstetrics (FIGO) staging system. Approval to review the patients’ medical records and pathological reports was obtained from the institutional review board of Fudan University Shanghai Cancer Center, Shanghai, China (050432-4-1911D). Written informed consent was obtained from all patients. All patients’ data were anonymized to avoid patient information identification during or after data collection.

Surgical procedure

Systemic staging involved hysterectomy, salpingo-oophorectomy, and pelvic and para-aortic lymphadenectomy. Omentectomy was performed in patients with grade 3 primary endometrioid uterine carcinoma and in those with non-endometrioid carcinoma. Radical hysterectomy was performed when the cervix was involved, which was confirmed using magnetic resonance imaging. Because the renal vein was routinely used as the upper margin for lymphadenectomy by our team, all node dissections were attempted to the level of the RVs regardless of the approach For laparoscopic procedures, the aortic and pelvic nodes were retrieved using a plastic specimen bag, which was extracted either vaginally (when hysterectomy was performed) or through a 15-mm port [1].

The procedure for extraperitoneal laparoscopic para-aortic lymphadenectomy was performed as previously reported, with simple modifications[20, 21]. Briefly, a 10-mm incision was made in the umbilicus for constant visual control during development of the extraperitoneal space. Then, to develop the extraperitoneal space, a 15-mm incision was placed 2 cm superomedially to the anterosuperior iliac spine. Once the peritoneal layer was visualized, the surgeon introduces one finger into the incision and performed blunt dissection to separate the peritoneal layer from the abdominal wall, under constant visual control via the umbilical port[20]. Once the extraperitoneal space was formed, a 15-mm trocar was inserted and gas was insufflated into the extraperitoneal space at a pressure of 12 to14 mmHg[20, 21]. A 5-mm and 10-mm trocar w placed at the midaxillary line, and another 5-mm trocar was placed if needed; four to five trocars were placed in total. Posteriorly, peritoneal marsupialization was performed to prevent the formation of lymph cysts.

The operating time was recorded from skin incision to closure, and included all procedures performed in each group. We also recorded the blood loss volumes for the three procedures. Postoperative complications were defined as any complications occurring within 90 days after surgery.

Statistical analysis

The patients’ age, body mass index (BMI), surgical stage, number of harvested para-aortic lymph nodes, surgical time, estimated blood loss and hospital stay were compared using the Mann-Whitney U test in each paired group. Fisher’s exact test was used to compare categorical variables between groups. A p-value of < 0.05 was considered statistically significant. MedCalc version 11.1.2.0 (MedCalc Software, Ostend, Belgium) was used for all statistical analyses.

We reviewed the data of 176 patients who underwent primary surgical staging treatment for endometrial cancer. The patients were divided into a transperitoneal laparoscopic para-aortic lymphadenectomy group (Group T, n = 21), laparotomic para-aortic lymphadenectomy group (Group L, n = 135), and extraperitoneal laparoscopic para-aortic lymphadenectomy group (Group E, n = 20). View from the left side during the extraperitoneal approach and position of each trocar placed is presented in Fig. 1.

The patients’ characteristics are summarized in Table 1. The patients’ median age at surgery was similar in Group T, Group L, and Group E (52, 54, and 55years, respectively; all comparisons, p > 0.05). The median BMI was also similar in Group T, L, and E (24.35, 24.22and 25.45 kgm², respectively; all comparisons, p > 0.05) The most common histological type was endometrioid adenocarcinoma in all groups, and Grade 1 was the most common tumor grade in all three groups. The FIGO stage was also comparable in the three groups (stage I and II vs stage III and IV, all comparisons, p > 0.05), and stage IA was the most common stage.

Table 1

Patients characteristics
Patient characteristics	group 1:transperitoneal	group 2:laporotomy	group 3:extropreitoneal	P value
	n = 21	n = 135	n = 20
Age at surgery,yrs
median(range)	52(39–70)	54(32–75)	55 (41–69)	All p > 0.05
BMI,kg/m2 (median,range)	24.35(16.9-32.51)	24.22(16.41–50.78)	25.45(21.19–32.51)	All p > 0.05
< 18 ,n(%)	1(4.76%)	1(0.74%)	0(0%)
18–25,n(%)	13(61.9%)	76(56.3%)	8(40%)
25–30,n(%)	6(28.57%)	45(33.33%)	10(50%)
30–35,n(%)	1(4.76%)	11(8.15%)	2(10%)
> 35,n(%)	0(0%)	2(1.48%)	0(0%)
Surgical stage				stage I and II vs stage III and IV All p>0.05
	14(66.67%)	90(66.67%)	12(60%)
IB	3(14.29%)	14(10.37%)	5(25%)
II	2(9.52%)	10(7.4%)	1(5%)
IIIA	2(9.52)	3(2.22%)	0(0%)
IIIB	0(0%)	1(0.74%)	0(0%)
IIIC1	0(0%)	11(8.15%)	1(5%)
IIIC2	0(0%)	4(2.96%)	1(5%)
IVA	0(0%)	0(0%)	0(0%)
IVB	0(0%)	(2.96%)	0(0%)
Histologic grade (G)
G1	9(42.86%)	55(40.74%)	9(45%)
G2	9(42.86%)	44(32.59%)	6(30%)
G3	1(4.76%)	19(9.63%)	3(15%)
UPSC	0(0%)	8(5.93%)	1(5%)
CCC	0(0%)	7(5.19%)	0(0%)
MMMT	0(0%)	0(0%)	0(0%)
Gx	2(9.52%)	0(0%)	0(0%)
Mixed epithelial carcinoma	0(0%)	1(0.74%)	0(0%)
Dedifferentiated carcinoma	0(0%)	10.74%)	1(5%)

The numbers of para-aortic nodes harvested via the different procedures are presented in Table 2. The median number of para-aortic lymph nodes was significantly higher in Group E than in Groups T and Group L (9.5, 5, and 6, respectively; p = 0.004 and = 0.0004, respectively). There was no significant difference between Group T and L (p = 0.581). Patients in Group L had more positive aortic nodes than patients in Groups T and E (30, 0, and 1 respectively). All patients in Group E underwent successful dissections to the RV level, and 71.43% and 94.07% of the patients in Groups T and L, respectively. The rate of dissection to the RV level was significantly higher in Groups L and E than in Group T (p = 0.0043 and p = 0.02, respectively), but the difference between Groups L and E was not statistically significant (p = 0.597). After limiting the count of removed lymph nodes to the group of patients who have dissected the para-aortic region up to the RV level, median number of harvested para-aortic node is 7, 6 and 9.5 in Groups T, L and E, respectively. Group E harvest more node than Group L (p = 0.0005), but not significantly different with Group T (p = 0.082).

Table 2

Patients characteristics of para-aortic node dissection via different procedure
	group1:transperitoneal	group2:laporotomy	group3:extropreitoneal
	n = 21	n = 135	n = 20
No. of para-aortic lymph nodes
median(range)	5(1–21)	6(1–19)	9.5 (5–29)
positive aortic nodes	0(0%)	30(22.22%)	1(5%)
cases with positive aortic nodes, no.(%)	0(0%)	6(4.44%)	1(5%)
cases with dissection to RV level	15(71.43%)	127(94.07%)	20(100%)

Perioperative and postoperative details are shown in Table 3. The median operation time was significantly shorter in Group L than in Groups T and E (96 minutes, 174 minutes, and 233minutes, respectively; p < 0.0001). The difference between Groups T and E was also significant (p = 0.001).

Table 3

Perioperative and postoperative characteristics
	group 1:transperitoneal	group 2:laporotomy	group 3:extropreitoneal	P Valule
	n = 21	n = 135	n = 20	group 1 vs group 2,P < 0.0001 group 1 vs group 3,P = 0.001 group 2 vs group 3,P < 0.0001
Surgical time,min
median(range)	174(93–275)	96(51–212)	233.5(145–309)
intraoperative complications,no(%)
urinary injury	1(4.76%)	2(1.48%)	0
estimated blood loss,ml median(range)	100(50–200)	200(50-1000)	142.5(50–300)	group 1 vs group 2,P < 0.0001 group 1 vs group 3,P > 0.05group 2 vs group 3༌P = 0.0086
Blood transfusion (unit)
mean(range)	0(0%)	0.17(0–4)	0
Surgical procedure
hysterectomy	19(90.48%)	117(86.67%)	19(95%)
radical hysterectomy	2(9.52%)	18(13.33%)	0(0%)
omentectomy	0(0%)	23(17.04%)	3(15%)
appendectomy	0(0%)	5(3.7%)	1(5%)
CRS	0(0%)	1(0.74%)	0(0%)
hospital stay,days
median(range)	5 (3–11)	6(4–21)	6(5–7)	group 1 vs group 2,P < 0.0001 group 1 vs group 3,P = 0.0781 group 2 vs group 3,P < 0.0001
postoperative complications
paralutic ileus	0(0%)	1(0.74%)	0(0%)
asymptomatic lymphocele	0(0%)	10(7.4%)	0(0%)
lymphedema	0(0%)	1(0.74%)	0(0%)

The estimated blood loss volumes were higher in Group L than in Groups T and E (200ml, 100ml, and 142.5ml, respectively; all comparisons, p < 0.001), but difference between Groups T and Group E was not statistically significant (p > 0.05).

The median length of hospital stay was significantly longer in Group L than in Groups T and E (6, 5 and6 respectively; all comparisons, p < 0.001). The length of hospital stay was similar in Groups T and E (p = 0.078).

Urinary injury was the most common intraoperative complication in Groups T and L, wheras no patients sustained a urinary injury in Group E. Patients in Group L developed the most postoperative complications, namely paralytic ileus (0.74%), asymptomatic lymphocele formation (7.4%), and lymphedema (0.74%). Only one patient was converted from Group E to Group T because of peritoneal leakage, and this patient was analyzed as part of Group T.

Thorough staging of endometrial carcinoma not only results in accurate documentation of disease spread, but is also a therapeutic intervention[13]. Minimally-invasive techniques have recently been proven safe alternatives for surgical staging, with less morbidity and quick recovery. The extraperitoneal laparoscopic lymphadenectomy approach provides equally favorable outcomes, especially regarding reaching the supramesenteric lymph nodes[5]. The upper limit of para-aortic lymphadenectomy must be the left renal vein because many studies have shown that clinically early endometrial carcinoma may have positive infrarenal nodes[12, 22, 23]. For this reason, our team routinely used the renal vein as the upper margin for lymphadenectomy.

The key finding of our study is that after comparing the transperitoneal, laparotomic, and extraperitoneal approaches, the extraperitoneal laparoscopic approach was most satisfactory for staging endometrial carcinoma, especially regarding para-aortic lymphadenectomy.

This study also showed that extraperitoneal laparoscopic para-aortic lymphadenectomy harvested higher numbers of para-aortic nodes than the other two approaches. This might because of the left-side extraperitoneal technique provides easier access to the left aortic nodes, which contains 63 % of all aortic nodes^{[16, 24]}.The extraperitoneal approach allows improved access to the left aortic lymph nodes, especially to the challenging supramesenteric nodal group without bowel interfering. A previous study suggested harvesting 5.3 to 21 aortic nodes. We harvested a median of9.5 para-aortic lymph nodes in Group E, 5 in Group T, and 6 in Group L. Pakish et al [25] reported a mean of 5 nodes harvested using the transperitoneal approach and 10 nodes using the extraperitoneal approach. The authors also indicated that extraperitoneal laparoscopy harvested significantly higher numbers of para-aortic lymph nodes than the transperitoneal approach. Dowdy et al.[20] found that the total number of harvested para-aortic lymph nodes was not significantly different between extraperitoneal laparoscopy and laparotomy. Although there was no difference in the rate of dissection to the RV level between Group L and Group E, these two approaches were significantly different in number of nodes harvest. Therefore, we believe that difference of removed lymph nodes numbers not only related to the level of lymph node dissection, but also related to the technique.

Removing more inframesenteric nodes significantly increases the likelihood of finding cancer, as does increasing the numbers of dissected infrarenal nodes [13]. Although we harvested more para-aortic lymph nodes in Group E, the percentage of positive nodes was higher in Group L. This result might be explained by the larger portion of grade 3 tumors and non-endometrial carcinomas in Group L, including papillary serous carcinoma, clear cell carcinoma, and malignant mixed mesodermal tumors, which are considered high-risk and more likely to metastasize to lymph nodes. Recently, increasingly more studies have been showing that lymphadenectomy does not benefit patients with grade 1 and 2 endometrioid lesions with myometrial invasion of ≤ 50% and a primary diameter of ≤ 2 cm.[26] Thus, performing more limited dissection of nodes or sentinel nodes, or even harvesting nodes might be safe in low-risk patients[27–29]. SLN mapping in early-staged EC has been demonstrated to be safe and accurate[29]. Low rate of lymph node metastasis in our results also support this, and limited node dissection might be adopted in our further work.

The time-consuming operation was a major disadvantage of the extraperitoneal approach in our study. Examination of the intraoperative outcomes revealed no significant difference in the total operative time between the groups in a previous study[5], similar to our results. The operative time in Group E was 30 minutes longer than that in Group T and 130 minutes longer than that in Group L. As reported previously, the extraperitoneal laparoscopic approach was associated with significantly shorter operative times for lymphadenectomy, whereas the total operative times were not different between the two groups[5]. The longer time might be related to the time required to prepare the retroperitoneal space. Previous studies showed that the total operative time with the extraperitoneal approach ranged from 200 to339.5 minutes[1, 18, 25], and our results were similar. Surgery in both Group T and Group E required more time than with laparotomy, which might reflect surgical skill.

The estimated blood loss volumes were lowest in Group T, and the length of hospital stay was shortest in Group E. Group L had significantly higher blood loss volumes and significantly longer hospital stays. These findings are consistent with the Gynecologic Oncology Group’s recommendation to perform minimally invasive approaches for endometrial cancer because of less blood loss and shorter length of hospital stay[7].

The most frequently reported postoperative complications after lymph node dissection are lymphocele and lymphedema[17], and paralytic ileus is also not uncommon. In Group E, we routinely performed peritoneal marsupialization to prevent the formation of lymph cysts. We found that Group E had few complications and low failure rates; only one patient required conversion to transperitoneal laparoscopy, similar to previous studies[20, 30].

Our study has several limitations the first limitation is the retrospective nature of the clinical data and the single-center design. Second, the sample size in Group E was small, and the small number of patients with a BMI of > 35 kg/m² limited the BMI-correlated subgroup analysis. Therefore, our results are limited to patients with a BMI of < 35 kg/m². Additionally, because we began performing extraperitoneal laparoscopy (Group E) only within 3 years of this study, we did not analyze overall survival in each group.

Our study showed that endometrial carcinoma staging via the extraperitoneal laparoscopic approach resulted in higher numbers of dissected para-aortic lymph nodes, longer surgical time, fewer intraoperative and postoperative complications, and shorter hospital stays than the laparotomy approach. The extraperitoneal laparoscopic approach should be considered for surgical staging of endometrial carcinoma.

Ethics approval and consent to participate

Approval to review the patients’ medical records and pathological reports was obtained from the institutional review board of Fudan University Shanghai Cancer Center, Shanghai, China. Written informed consent was obtained from all patients.

Consent to publication

Written informed consent was obtained from the patient for publication and accompanying images. A copy of the written consent is available for review by the Editor of this journal.

Availability of data and materials

The dataset supporting the conclusions of this article is included within the article and its additional file.

Competing interests

The authors declare no competing interests.

Funding

Wei Zhang is supported by the National Natural Science Foundation of China (81602270). The service fee of the researchers in our study was supported by this funding.

Authors' contributions

Category I
(1) Conception and Design
CXJ;WXH
(2) Data Acquisition
XLF;WH;JXZ
(3) Data analysis and interpretation
HXT;YHJ

Category II
(1) Drafting the article
ZW
(2) Revising it critically for important intellectual content
ZW;CXJ
Category III
(1) Final approval of the version to be published
CXJ;WXH
Category IV
(1) Agreement to be accountable for all aspects of the work
WXH

All authors have read and approved the manuscript.

Acknowledgments
Not applicable

Diaz-Feijoo B, Correa-Paris A, Perez-Benavente A, Franco-Camps S, Sanchez-Iglesias JL, Cabrera S, de la Torre J, Centeno C, Puig OP, Gil-Ibanez B, et al. Prospective Randomized Trial Comparing Transperitoneal Versus Extraperitoneal Laparoscopic Aortic Lymphadenectomy for Surgical Staging of Endometrial and Ovarian Cancer: The STELLA Trial. Ann Surg Oncol. 2016;23:2966–74.
Walker JL, Piedmonte MR, Spirtos NM, Eisenkop SM, Schlaerth JB, Mannel RS, Spiegel G, Barakat R, Pearl ML, Sharma SK. Laparoscopy compared with laparotomy for comprehensive surgical staging of uterine cancer: Gynecologic Oncology Group Study LAP2. J Clin Oncol. 2009;27:5331–6.
Vasilev SA, McGonigle KF. Extraperitoneal laparoscopic paraaortic lymph node dissection: development of a technique. J Laparoendosc Surg. 1995;5:85–90.
Querleu D, Dargent D, Ansquer Y, Leblanc E, Narducci F. Extraperitoneal endosurgical aortic and common iliac dissection in the staging of bulky or advanced cervical carcinomas. Cancer. 2000;88:1883–91.
Prodromidou A, Machairas N, Spartalis E, Kostakis ID, Iavazzo C, Moris D, Tsilimigras DI, Athanasiou A, Nikiteas N. Transperitoneal Versus Extraperitoneal Laparoscopic Lymphadenectomy for Gynecological Malignancies: A Systematic Review and Meta-analysis. Anticancer Res. 2018;38:4677–81.
Ferron G, De Santiago J, Querleu D, Martinez A, Angeles MA, Boulet B, Guyon F, Zapardiel I. Left Lateral Endosurgical Extraperitoneal Total Hysterectomy with Para-Aortic and Pelvic Lymphadenectomy: A Novel Approach for the Obese Patient with Endometrial Cancer. J Minim Invasive Gynecol. 2018;25:730–6.
Narducci F, Lambaudie E, Mautone D, Hudry D, Bresson L, Leblanc E. Extraperitoneal Para-aortic Lymphadenectomy by Robot-Assisted Laparoscopy in Gynecologic Oncology: Preliminary Experience and Advantages and Limitations. Int J Gynecol Cancer. 2015;25:1494–502.
Soliman PT, Frumovitz M, Spannuth W, Greer MJ, Sharma S, Schmeler KM, Ramirez PT, Levenback CF, Ramondetta LM. Lymphadenectomy during endometrial cancer staging: practice patterns among gynecologic oncologists. Gynecol Oncol. 2010;119:291–4.
Heller PB, Maletano JH, Bundy BN, Barnhill DR, Okagaki T. Clinical-pathologic study of stage IIB, III, and IVA carcinoma of the cervix: extended diagnostic evaluation for paraaortic node metastasis–a Gynecologic Oncology Group study. Gynecol Oncol. 1990;38:425–30.
Franchi M, Garzon S, Zorzato PC, Laganà AS, Casarin J, Locantore L, Raffaelli R, Ghezzi F. PET-CT scan in the preoperative workup of early stage intermediate- and high-risk endometrial cancer. Minim Invasive Ther Allied Technol. 2020;29:232–9.
Ramirez PT, Jhingran A, Macapinlac HA, Euscher ED, Munsell MF, Coleman RL, Soliman PT, Schmeler KM, Frumovitz M, Ramondetta LM. Laparoscopic extraperitoneal para-aortic lymphadenectomy in locally advanced cervical cancer: a prospective correlation of surgical findings with positron emission tomography/computed tomography findings. Cancer. 2011;117:1928–34.
Turan T, Yilmaz SS, Hizli D, Gundogdu B, Boran N, Tulunay G, Ozfuttu A, Kose MF. A prospective evaluation of lymphatic dissemination in endometrial cancer: is it adequate to perform lymph node dissection up to the inferior mesenteric artery? Int J Gynecol Cancer. 2011;21:864–9.
O'Hanlan KA, Sten MS, O'Holleran MS, Ford NN, Struck DM, McCutcheon SP. Infrarenal lymphadenectomy for gynecological malignancies: two laparoscopic approaches. Gynecol Oncol. 2015;139:330–7.
Todo Y, Kato H, Minobe S, Okamoto K, Suzuki Y, Sudo S, Takeda M, Watari H, Kaneuchi M, Sakuragi N. Initial failure site according to primary treatment with or without para-aortic lymphadenectomy in endometrial cancer. Gynecol Oncol. 2011;121:314–8.
Morice P, Joulie F, Camatte S, Atallah D, Rouzier R, Pautier P, Pomel C, Lhomme C, Duvillard P, Castaigne D. Lymph node involvement in epithelial ovarian cancer: analysis of 276 pelvic and paraaortic lymphadenectomies and surgical implications. J Am Coll Surg. 2003;197:198–205.
Michel G, Morice P, Castaigne D, Leblanc M, Rey A, Duvillard P. Lymphatic spread in stage Ib and II cervical carcinoma: anatomy and surgical implications. Obstet Gynecol. 1998;91:360–3.
Morales S, Zapardiel I, Grabowski JP, Hernandez A, Diestro MD, Gonzalez-Benitez C, De Santiago J. Surgical outcome of extraperitoneal paraaortic lymph node dissections compared with transperitoneal approach in gynecologic cancer patients. J Minim Invasive Gynecol. 2013;20:611–5.
Akladios C, Ronzino V, Schrot-Sanyan S, Afors K, Fernandes R, Baldauf JJ, Wattiez A. Comparison between transperitoneal and extraperitoneal laparoscopic paraaortic lymphadenectomy in gynecologic malignancies. J Minim Invasive Gynecol. 2015;22:268–74.
Narducci F, Lambaudie E, Houvenaeghel G, Collinet P, Leblanc E. Early experience of robotic-assisted laparoscopy for extraperitoneal para-aortic lymphadenectomy up to the left renal vein. Gynecol Oncol. 2009;115:172–4.
Dowdy SC, Aletti G, Cliby WA, Podratz KC, Mariani A. Extra-peritoneal laparoscopic para-aortic lymphadenectomy–a prospective cohort study of 293 patients with endometrial cancer. Gynecol Oncol. 2008;111:418–24.
Gorostidi M, Diaz-Feijoo B. Concerns about robotic extraperitoneal para-aortic lymphadenectomy as isolated procedure: is it worth it? Int J Gynecol Cancer. 2015;25:192.
Scribner DR Jr, Walker JL, Johnson GA, McMeekin SD, Gold MA, Mannel RS. Laparoscopic pelvic and paraaortic lymph node dissection: analysis of the first 100 cases. Gynecol Oncol. 2001;82:498–503.
Burke TW, Levenback C, Tornos C, Morris M, Wharton JT, Gershenson DM. Intraabdominal lymphatic mapping to direct selective pelvic and paraaortic lymphadenectomy in women with high-risk endometrial cancer: results of a pilot study. Gynecol Oncol. 1996;62:169–73.
Morice P, Joulie F, Camatte S, Atallah D, Rouzier R, Pautier P, Pomel C, Lhommé C, Duvillard P, Castaigne D. Lymph node involvement in epithelial ovarian cancer: analysis of 276 pelvic and paraaortic lymphadenectomies and surgical implications. J Am Coll Surg. 2003;197:198–205.
Pakish J, Soliman PT, Frumovitz M, Westin SN, Schmeler KM, Reis RD, Munsell MF, Ramirez PT. A comparison of extraperitoneal versus transperitoneal laparoscopic or robotic para-aortic lymphadenectomy for staging of endometrial carcinoma. Gynecol Oncol. 2014;132:366–71.
Mariani A, Dowdy SC, Cliby WA, Gostout BS, Jones MB, Wilson TO, Podratz KC. Prospective assessment of lymphatic dissemination in endometrial cancer: a paradigm shift in surgical staging. Gynecol Oncol. 2008;109:11–8.
Bogani G, Murgia F, Ditto A, Raspagliesi F. Sentinel node mapping vs. lymphadenectomy in endometrial cancer: A systematic review and meta-analysis. Gynecol Oncol. 2019;153:676–83.
Rossi EC, Kowalski LD, Scalici J, Cantrell L, Schuler K, Hanna RK, Method M, Ade M, Ivanova A, Boggess JF. A comparison of sentinel lymph node biopsy to lymphadenectomy for endometrial cancer staging (FIRES trial): a multicentre, prospective, cohort study. Lancet Oncol. 2017;18:384–92.
Zorzato PC, Bosco M, Franchi MP, Mariani A, Cianci S, Garzon S, Uccella S. Sentinel lymph-node for endometrial cancer treatment: review of literature. Minerva Med 2020.
Diaz-Feijoo B, Gil-Ibanez B, Perez-Benavente A, Martinez-Gomez X, Colas E, Sanchez-Iglesias JL, Cabrera-Diaz S, Puig-Puig O, Magrina JF, Gil-Moreno A. Comparison of robotic-assisted vs conventional laparoscopy for extraperitoneal paraaortic lymphadenectomy. Gynecol Oncol. 2014;132:98–101.

Additionalfile1.xlsx
Supporting information Additional file 1

Download PDF

Editorial decision: Major Revision
01 Sep, 2021
Review #4 received at journal
31 Aug, 2021
Review #5 received at journal
31 Aug, 2021
Review #3 received at journal
29 Aug, 2021
Review #2 received at journal
28 Aug, 2021
Review #1 received at journal
23 Aug, 2021
Reviewer #5 agreed at journal
20 Aug, 2021
Reviewer #4 agreed at journal
19 Aug, 2021
Reviews received at journal
17 Aug, 2021
Reviewer #3 agreed at journal
16 Aug, 2021
Reviewer #2 agreed at journal
16 Aug, 2021
Reviewer #1 agreed at journal
10 Aug, 2021
Reviewers invited by journal
08 Apr, 2021
Editor assigned by journal
07 Apr, 2021
Editor invited by journal
07 Apr, 2021
Submission checks completed at journal
07 Apr, 2021
First submitted to journal
07 Apr, 2021

You are reading this latest preprint version

Extraperitoneal Laparoscopy for Para-Aortic Lymphadenectomy in Endometrial Carcinoma Staging: An Approach with Higher Efficiency

Status:

Version 1

Abstract

Figures

Background

Methods

Patients and inclusion criteria

Surgical procedure

Statistical analysis

Results

Discussion

Conclusion

Declarations

References

Supplementary Files

Status:

Version 1