Arch Gynecol Obstet DOI 10.1007/s00404-015-3814-y
REVIEW
Robotic retroperitoneal lymph node dissection in gynaecological neoplasms: comparison of extraperitoneal and transperitoneal lymphadenectomy Christos Iavazzo1,2 • Ioannis D. Gkegkes3
Received: 17 March 2015 / Accepted: 3 July 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Objective The main aim of our study is to review the till now available literature data on the role of robotic retroperitoneal lymph node dissection in gynaecological cancers by comparing the extraperitoneal versus the transperitoneal approach. Methods A thorough and systematic search was performed in electronic databases of PubMed and Scopus. Results The extraperitoneal approach is described in 148 patients. The age of the patients ranged from 26 to 78 years. The indications included cervical, endometrial and ovarian carcinoma in 113, 22 and 12 patients, respectively. The operative time ranged between 45 and 410 min. The number of dissected lymph nodes ranged from 3 to 25, while only 13 of them were found to be positive. The mean estimated blood loss during the operation was 77 ml (range \50–200 ml). Seven cases were converted to open. The duration of hospital stay ranged from 2 to 14 days. The transperitoneal approach is described in 898 patients. The age of the patients ranged from 15 to 89 years. Cervical, endometrial and ovarian carcinomas were the principal neoplasias present in 248, 449 and 164 patients, respectively. The operative time ranged from 19 to 633 min. The number of dissected lymph nodes ranged from 1 to 54, while the total number of patients with positive lymph nodes dissected was 56 & Christos Iavazzo [email protected] 1
Gynaecological Oncology Department, Christie Hospital, Manchester, UK
2
38, Seizani Str., Nea Ionia, 14231 Athens, Greece
3
First Department of Surgery, General Hospital of Attica ‘‘KAT’’, Athens, Greece
patients. The estimated blood loss during the operation varied between 20 and 1800 ml. Only 9 out of 898 patients were converted to open. The duration of hospital stay ranged from 1 to 40 days. Conclusion A reliable definition of the ‘‘kind’’ of lymphadenectomy used in each study is the first step in order to reach safe conclusions. The lack of comparative studies, especially the randomized ones, cannot help us draw any safe conclusion regarding both the clinical outcomes and the possibility of any superiority of these different approaches (extraperitoneal and transperitoneal). Keywords Robotics Lymphadenectomy Retroperitoneal Extraperitoneal Transperitoneal Gynaecological cancer
Introduction The main role of lymph node dissection is to decrease or even better eradicate the risk of recurrence [1]. Furthermore, lymph node dissection may also provide more information about disease staging or it may lead to the early recognition of lymph node metastases, offering the opportunity to the patient to start earlier the adjuvant therapy. The lymphadenectomy in gynaecological malignancies is controversial, and several studies are ongoing to answer the question of should we or should we not dissect systematically the lymph nodes in cancers as endometrium or ovarian cancer. More specifically, the Gynecologic Oncology Group (GOG)—Protocol 33 showed that patients with endometrial cancer can have extra-uterine disease in 22 % of the cases including disease spread to pelvic lymph nodes in 9 % and para-aortic lymph nodes in 5 % [2]. For this reason, the International
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Federation of Gynecology and Obstetrics (FIGO) included pelvic and para-aortic lymph node status in the surgical staging system for endometrial cancer. It is shown that the performance of pelvic and para-aortic lymph node dissection can lead to diagnostic and therapeutic advantages [3, 4]. However, lymph node dissection as a part of endometrial cancer staging, especially in low-risk patients, is still controversial. Regarding cervical cancer, the status of pelvic and para-aortic lymph nodes is one of the most important prognostic factors which also affects the extent of the radiation field [5–7]. GOG study showed that the 3-year disease-free interval was 74 % for those with positive nodes versus 86 % for node-negative patients with stage IB cervical cancer [5]. It is accepted that a more thorough lymph node dissection could increase the likelihood of detecting occult metastatic disease. Recently, Shah et al. showed that the extent of lymph node dissection in women with early-stage cervical cancer influences survival as node-negative patients have better survival when a greater number of lymph nodes are dissected [8]. In ovarian cancer patients, the role of lymph node dissection has been debated. Retroperitoneal lymph node involvement occurs in 5–25 and 50–80 % of women with early and advanced ovarian cancer, respectively. Retrospective studies showed that lymph node dissection is associated with an improvement of staging, complete cytoreduction and a survival benefit, even though current ongoing prospective trial on ovarian cancer (LION study) will help give a definitive answer on this issue and investigate if these data—especially the node ratio—have therapeutic implications and may be considered in future staging [9–12, 37]. Minimally invasive techniques have become the gold standard of care as they decrease morbidity, hospital stay and period of return to normal activity. They have also been used for retroperitoneal lymph node dissection with comparable outcomes regarding the number of lymph nodes and prognosis. The majority of the cases are performed with the transperitoneal approach; however, recently extraperitoneal approach has been widely used. Robotic technology is characterized by the three-dimensional view, the infiltration of surgeon’s natural tremor, the improved dexterity and less operator fatigue, and for this reason the important role that a robotic approach can have in the lymph node dissection is highlighted [13, 14]. The main aim of our study is to review the till now available literature data on the role of robotic technique in extraperitoneal and transperitoneal lymph node dissection of patients with gynaecological cancers.
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Methods Data sources A thorough and systematic search was performed in electronic databases of PubMed (28 April 2015) and Scopus (28 April 2015). The search strategy adopted at the aforementioned databases was based on a combination of keywords: (robot OR robotic OR telesurgery) AND (retroperitoneal OR transperitoneal OR extraperitoneal) AND (lymphadenectomy OR lymph node dissection). The references of the included articles were also searched for additional studies. Study selection criteria In this review, all the studies that reported data relevant on the role of robotics in both extraperitoneal and transperitoneal lymph node dissection were included. Abstracts from conferences, letters to the editor, surveys, review articles and animal studies were not included in the analysis. Papers published in other languages than English, Spanish, German, French, Italian or Greek were excluded.
Results A total of 107 and 540 search results were retrieved during the performed search in PubMed and Scopus databases, respectively, among of which 18 studies were identified as eligible for inclusion in our review [15–28, 39–41]. One additional study was identified through hand-searching of references [38]. In Fig. 1, the included studies are represented graphically (flow diagram). The major characteristics of the included studies in our review (number of patients included, age of patients, patients’ body mass index, histological type of tumour, clinical stage of the primary cancer, history of previous radiotherapy/chemotherapy, duration of operative time, number of dissected lymph nodes, number of positive lymph nodes, estimated blood loss during lymph node dissection, cases of conversion to open, complications (intra- or post-operative), intra-operative need of transfusion, duration of hospital stay, duration of follow-up and the presence of recurrence during follow-up) are presented in Tables 1 and 2. Regarding the extraperitoneal lymphadenectomy, the literature search revealed 6 case series and 2 case reports. In total, 148 patients were included in our review. The age of the patients ranged from 26 to 78 years. The body mass
Arch Gynecol Obstet Fig. 1 Flow diagram that presents in detail the selection process of the included articles in our review
index (BMI) of the patients ranged from 19 to 48.83 kg/m2. Cervical, endometrial and ovarian carcinomas were present in 113, 22 and 12 patients, respectively. A history of radiotherapy and a combination of radio/chemotherapy was present in 2 and 2, respectively. The majority of the included carcinomas were of low clinical stage. Specifically, in cases of cervical carcinoma, the greatest part of the patients was up to stage IIB (59 out of 113), while 33 out of 113 patients presented a clinical stage superior to IIB. The major part of the patients with endometrial cancer was inferior to stage III (7 out of 22). The main clinical stage of the patients with ovarian carcinoma was stage I (2 out of 12). The operative time ranged between 45 and 410 min. The number of dissected lymph nodes ranged from 3 to 25, while only 13 of them were found to be positive to neoplasia. The mean estimated blood loss during the operation was 77 ml (range \50–200 ml). Seven cases of conversion to open were reported due to poor visibility (1 out of 7), loss of the pneumo-retroperitoneum (1 out of 7), injury of the left ureter (1 out of 7), major bleeding (2 out of 7), enlarged uterus (1 out of 7) and the need to perform Bricker procedure (1 out of 7). Among the intra-operative complications, ureteral injury, vascular injury and pneumothorax were found in 3, 4 and 1 patients, respectively. Regarding the post-operative complications, seven cases of lymphocysts, one case of digestive fistula, one case of plexus brachial paralysis, one case of pulmonary embolism, one case of surgical site infection, one case of urinoma, two cases of haematoma and two cases of lymphocele were reported. The necessity of transfusion was present only in two patients without any reference to the quantity of the blood loss. The duration of hospital stay ranged from 2 to 14 days. None of the included patients presented disease recurrence during the follow-up period which was not mentioned in none of the included studies.
Regarding the most widely used transperitoneal lymphadenectomy, the utilized search strategy revealed 11 case series and 3 case reports. In our review, 898 patients were included. The age of the patients ranged from 15 to 89 years. The BMI of the patients ranged from 16 to 57 kg/m2. Cervical, endometrial and ovarian carcinomas were the principal neoplasias present in 248, 449 and 164 patients, respectively. A history of radiotherapy, chemotherapy and a combination of radio/chemotherapy was present in 3, 8 and 7 patients, respectively. The majority of the included carcinomas were of low clinical stage. In particular, in cases of cervical carcinoma, the large part of the patients was of stage IB2 (114 out of 248), while the major part of patients with endometrial cancer was inferior of stage II. The clinical stage of the patients with ovarian carcinoma ranged between stage IA and IIIB (72 out of 164). The operative time ranged from 19 to 633 min. The number of dissected lymph nodes ranged from 1 to 54, while the total number of patients with positive lymph nodes dissected was 56. The estimated blood loss during the operation varied between 20 and 1800 ml. Only in 9 out of 898 patients, the conversion to open was reported because of vascular injury (5 out of 9), bowel injury (2 out of 9) and poor visibility (2 out of 9). The most common intra-operative complications were vascular injuries and bleeding present in 8 and 2 patients, respectively. The most common post-operative complications included lymphocysts, lymphocele, chylous ascites, port-site hernia and haematoma, which were found in 25, 13, 10, 4 and 3 patients, respectively. Transfusion was required in 31 patients (for blood loss over 500 ml). The duration of hospital stay ranged from 1 to 40 days. The follow-up period ranged between 1 and 56 months. Disease recurrence during follow-up was found only in 10 patients.
123
123
Hudry [40]
Akladios [41]
Case series
References
Mean (range): 26.6 (16.2–50) Mean (range): 22.5 (16.63–35)$
Mean (range): 58 (15–89)
Mean (range): 49 (23–79)$
429#
Mean (range): 26.9 (19–48), p = 0.09
Mean (range): 55.2 (38–75), p = 0.53
21##
Mean (range): 23.5 (16–35)
BMI (in kg/m2)
Mean (range): 53.3 (19–78)
Age of patient (in y.o.)
51#
Nr of patients
Other: 9/429 (2)
Cervical cancer: 107/429 (25)
Ovarian/tubal cancer: 60/429 (14),
Endometrial cancer: 253/429 (59),
Cervical cancer: 16/21 (76.3), p = 0.028
Ovarian cancer: 3/21 (14.3),
Endometrial cancer: 1/21 (4.8),
Unknown: 2/429 (0.5)
IVA: 3/429 (1)
IIIB: 4/429 (1)
IIIA: 4/429 (1)
IIB: 39/429 (9)
IIA: 4/429 (1)
IB1: 32/429 (7.5) IB2: 17/429 (4)
IA2: 1/429 (0.5)
Cervical cancer: IA1: 1/429 (0.5)
IV: 4/429 (1)
IIIC: 32/429 (7.5)
IIIA: 23/429 (5.4)
II: 18/429 (4)
IB: 115/429 (27)
Endometrial cancer: IA: 59/429 (14)
NM
NM
RTh/CTh: 2/21 (9.5)
CTh: 0/21
RTh: 2/21 (9.5)
RTh/CTh: 7/51 (14)
Cervical cancer: 22/51 (44)
RTh: 2/51 (4)
Previous RTh/CTh (%)
CTh: 8/51 (16)
NM
Clinical stage of primary neoplasia (%)
Ovarian cancer: 20/51 (40),
Endometrial cancer: 8/51 (16),
Histological type (%)
Table 1 Studies reporting data regarding the robot-assisted retroperitoneal lymph node dissection
Mean (SD): 200.4 (66)
Mean (range): 125.7 (45–180), p = 0.001
Mean (range): 200.2 (35–360)
Operative time (in min)
Mean (SD): 16.6 (8.9)
Mean (range): 13 (3–25), p = 0.015
Mean (range): 17 (4–37)
Nr of dissected LNs
Arch Gynecol Obstet
Bats [15]
References
Median (IQR): 55 (42–64)
Median (IQR): 24.1 (20.9–26.1)
Mean (range): 25 (19–48.83)$
Mean (range): 52 (27–74)$
24
Mean (range): 26.6 (20.82–33.2)
Mean (range): 62 (26–74)
58##
BMI (in kg/m2)
Age of patient (in y.o.)
Nr of patients
Table 1 continued
IIIB: 1/25 (4)
IC: 1/25 (4)
Ovarian cancers:
IIIC: 2/25 (8)
II: 1/25 (4)
IB: 2/25 (8)
IVA: 1/25 (4) Endometrial cancers: IA: 2/25 (8)
IIIB: 1/25 (4)
IIIA: 1/25 (4)
IIB: 5/25 (20)
IIA: 2/25 (8)
IB2: 2/25 (8)
Endometrial carcinoma: 8/25 (32) Ovarian carcinoma: 2/25 (8)*
Cervical cancers: IB1: 1/25 (4)
IVA: 2/58 (3.5)
IIIB: 2/58 (3.5)
IIIA: 5/58 (1)
IIA: 6/58 (1.4) IIB: 27/58 (47)
IB2: 8/58 (2)
IB1: 1/58 (1.7)
Cervical cancer:
Unknown: 2/58 (3.5)
IV: 4/58 (7)
IIIC: 2/58 (3.5)
Endometrial cancer: IA: 2/58 (3.5)
Clinical stage of primary neoplasia (%)
Cervical carcinoma: 15/25 (60)
Cervical cancer: 50/58 (86)
Ovarian/tubal cancer: 4/58 (7),
Endometrial cancer: 4/58 (7),
Histological type (%)
–
NM
Previous RTh/CTh (%)
Median (IQR): 240 (180–300)
Mean (SD): 177.1 (62.7), p = 0.054
Operative time (in min)
Median (range): 18 (14–25)
Mean (SD): 18.3 (9.4), p = 0.32
Nr of dissected LNs
Arch Gynecol Obstet
123
123
13
7
15
Gorostidi [20]
Fastrez [18]
Lambaudie [22]
5
5
Narducci [24]
Vergote [26]
Case reports
Nr of patients
References
Table 1 continued
21.5 28.8 25.2
45
74
62
25
56 24.4
25
49
40
29
65
19.3
23
27
24
61
Mean (SD): 27.4 (5.16)
Median (range): 24 (19–29)
Median (range): 31.9 (20–41.5)
BMI (in kg/m2)
28
Mean (SD): 49 (11.3)
Median (range): 50.5 (27–74)
Median (range): 60.3 (42–78)
Age of patient (in y.o.)
IIB: 1/13 (7.7)
Endometrial carcinoma: 9/13 (69.2)
IIA: 1/15 (6.7) IIB: 5/15 (33.3) IIIA: 1/15 (6.7)
Ovarian/tubal cancer 1/15 (6.7) Lymph node recurrence: 1/15 (6.7)
Cervical SCC
Cervical SCC
IIB
IIIB
IIB
IIB
IIB
NM
NM
NM
IIB
NM
73
60
65
82
139
130
215
165
235
240
IB2: 6/15 (40),
–
Mean (SD): 202.1 (64)
NM
Cervical cancer
Cervical cancer 13/15 (86.7)
IIB
Median (range): 100 (60–140)
NM
Cervical carcinoma
[IB2
IA: 1/13 (7.7)
Ovarian carcinoma:
IB: 1/13 (7.7)
IA: 8/13 (61.5)
Endometrial carcinoma:
IIIB: 1/13 (7.7)
Mean (range): 323 (180–410)
NR
Cervical carcinoma:
Cervical carcinoma: 2/13 (15.4)
Ovarian carcinoma: 2/13 (15.4)
Operative time (in min)
Previous RTh/CTh (%)
Clinical stage of primary neoplasia (%)
Histological type (%)
12
9
7
9
9
12
20
17
11
9
Mean (SD): 16.7 (8)
Median (range): 9.5 (7–12)
Median (range): 12 (4–21)
Nr of dissected LNs
Arch Gynecol Obstet
NM
NM
Fastrez [18]
Lambaudie [22]
Case reports
–
Gorostidi [20]
Mean (SD): 70.9 (69.3)
NM
NM
NM
Mean (SD): 113.5 (132.8), p = 0.28
NM
NM
Mean (SD): 149.8 (118.8)
NM
8/21 (38), p = 0.01
NM
NM
EBL (in ml)
6/52 (11.6)
Nr of positive LNs
Bats [15]
Hudry [40]
Akladios [41]
Case series
References
Table 1 continued
–
–
1
3
0/58, p = 0.39
4/429 (1)
3/21 (14.2)
1/51 (1.3)
Conversion to open
Haematoma: 1/15 (6.7)
Post-op:
Ureteral injury: 1/7 (14.3)
Intra-op:
Lymphocele: 1/13 (7.7)
Urinoma: 1/13 (7.7)
SSI: 1/13 (7.7)
Post-op:
IMA rupture: 1/13 (7.7)
Intra-op:
Lymphocele: 1/24 (4) Pulmonary embolism: 1/24 (4)
Blood transfusion: 1/24 (4)
Plexus brachial paralysis: 1/24 (4)
Digestive fistula: 1/24 (4)
Post-op:
Transaction of renal lower pole artery: 1/24 (4)
Bilateral PNX: 1/24 (4)
Intra-op:
Lymphocyst: 7/58 (12)$$
l Post-op:
Post-op: Lymphocyst: 25/429 (6)
Vessel injuries: 2/21 (9.5)
Urinary injuries: 1/21 (4.8)
Vessel injuries: 2/51 (4)
Urinary injuries: 1/51 (2)
Bowel injuries: 2/51 (4)
Complications (intra-op or post-op) (%)
N
N
Y: 1/13
N
Y: 10/487
Y: 1/5, p = 0.26
Y: 9/18
Transfusion (Y/N)
NM
NM
NM
NM
NM
NM
NM
NM
Follow up (in mo)
Mean (SD): 2.6 (0.6)
Median (range): 2.5 (2–3)
Mean: 3.4
Median (IQR): 5 (4–8)
Mean (SD): 2.7 (0.8), p = 0.001
Mean (SD): 3.5 (1.9)
Mean (range): 5.6 (2–14), p = 0.049
Mean (range): 7.7 (2–40)
Hospital stay (in days)
NM
NM
NM
NM
NM
NM
NM
NM
Recurrence
Arch Gynecol Obstet
123
123 50 50 50 50 50
5 –
–
–
–
Vergote [26]
–
–
–
Ureteral injury:
– Intra-op:
– N
N
Transfusion (Y/ N)
NM
NM
Follow up (in mo)
2
2
2
2 3
NM
Hospital stay (in days)
NM
NM
Recurrence
$$
$
##
#
*
In overall, regarding the total complications, no differences were found between the two groups (p = 0.31)
Lymphadenectomy as isolated procedure
Retroperitoneal group
One patient had both endometrial and ovarian cancers Transperitoneal group
USA United States of America, y.o. years old, BMI body mass index, Nr number, EBL estimated blood loss, N No, Y yes, IMA inferior mesenteric artery, RTh radiotherapy, CTh chemotherapy, mo months, NM not mentioned, SCC squamous cell carcinoma, LN lymph node, SSI surgical site infection, IQR interquartile range, PNX pneumothorax
–
Post-op: Lymphocele, seroma/haematoma
–
50 \50
–
–
Complications (intra-op or post-op) (%)
50
–
Conversion to open
180
200
–
Narducci [24]
EBL (in ml)
Nr of positive LNs
References
Table 1 continued
Arch Gynecol Obstet
Hudry [40]
Akladios [41]
Case series
References
Mean (range): 26.6 (16.2–50) Mean (range): 22.5 (16.63–35)$
Mean (range): 55.2 (38–75), p = 0.53
Mean (range): 58 (15–89)
Mean (range): 49 (23–79)$
21##
429#
Mean (range): 26.9 (19–48), p = 0.09
Mean (range): 53.3 (19–78)
Mean (range): 23.5 (16–35)
Age of patient (in y.o.) BMI (in kg/m2)
51#
Nr of patients
Other: 9/429 (2)
Cervical cancer: 107/429 (25)
Ovarian/tubal cancer: 60/429 (14),
Endometrial cancer: 253/429 (59),
Cervical cancer: 16/21 (76.3), p = 0.028
Ovarian cancer: 3/21 (14.3),
Endometrial cancer: 1/21 (4.8),
Cervical cancer: 22/51 (44)
Ovarian cancer: 20/51 (40),
Endometrial cancer: 8/51 (16),
Histological type (%)
Table 2 Studies reporting data regarding the robot-assisted transperitoneal lymph node dissection
Unknown: 2/429 (0.5)
IVA: 3/429 (1)
IIIB: 4/429 (1)
IIIA: 4/429 (1)
IIB: 39/429 (9)
IIA: 4/429 (1)
IB1: 32/429 (7.5) IB2: 17/429 (4)
IA2: 1/429 (0.5)
Cervical cancer: IA1: 1/429 (0.5)
IV: 4/429 (1)
IIIC: 32/429 (7.5)
IIIA: 23/429 (5.4)
II: 18/429 (4)
IB: 115/429 (27)
Endometrial cancer: IA: 59/429 (14)
NM
NM
Clinical stage of primary neoplasia (%)
NM
RTh/CTh: 2/21 (9.5)
CTh: 0/21
RTh: 2/21 (9.5)
RTh/CTh: 7/51 (14)
CTh: 8/51 (16)
RTh: 2/51 (4)
Previous RTh/CTh (%)
Mean (SD): 200.4 (66)
Mean (range): 125.7 (45–180), p = 0.001
Mean (range): 200.2 (35–360)
Operative time (in min)
Mean (SD): 16.6 (8.9)
Mean (range): 13 (3–25), p = 0.015
Mean (range): 17 (4–37)
Nr of dissected LNs
Arch Gynecol Obstet
123
123
Kimmig [38]
Median (range): 46 (31–71)
19
Median (range): 54.5 (36–73)
8§
Median (range): 59 (26–78)
Median (range): 55 (32–78)
22
16
Median (IQR): 59 (38.6–66.3), p = 0.408
30
Fastrez [18]
Median (IQR): 57.5 (47.5–66.7)
32
Coronado [17]
Mean (SD): 65.6 (11.3)
Median (range): 23 (18–33)
Median (range): 32 (20–57)
Median (range): 24.5 (17–32)
Median (range): 27 (17–37)
Median (IQR): 25 (21.6–27.1), p = 0.193
Median (IQR): 25.4 (21.6–30.4)
Mean (SD): 31.9 (7.1)
Mean (range): 25 (19–48.83)$
Mean (range): 52 (27–74)$
97
Mean (range): 26.6 (20.82–33.2)
Mean (range): 62 (26–74)
58##
BMI (in kg/m2)
Age of patient (in y.o.)
Nr of patients
James [39]
References
Table 2 continued
Cervical carcer
Endometrial cancer:
Cervical carcer
Cervical cancer: 30/62 (48.4)
Ovarian cancer: 12/62 (19.4),
Endometrial cancer: 20/62 (32.2),
Endometrial cancer
Cervical cancer: 50/58 (86)
Ovarian/tubal cancer: 4/58 (7),
Endometrial cancer: 4/58 (7),
Histological type (%)
II: 1/19 (5)
I: 18/19 (95)
III: 3/16 (9)
I: 13/16 (81)
[IB2
NM
IIIC2: 18/97 (18.6)
IIIC1: 21/97 (21.7)
IIIB: 1/97 (1)
IIIA: 1/97 (1)
IB: 17/97 (17.5) II: 4/97 (4.1)
IA: 35/97 (36.1)
IVA: 2/58 (3.5)
IIIB: 2/58 (3.5)
IIIA: 5/58 (1)
IIB: 27/58 (47)
IIA: 6/58 (1.4)
IB2: 8/58 (2)
IB1: 1/58 (1.7)
Cervical cancer:
Unknown: 2/58 (3.5)
IV: 4/58 (7)
IIIC: 2/58 (3.5)
Endometrial cancer: IA: 2/58 (3.5)
Clinical stage of primary neoplasia (%)
NM§§§
NM§§
NM
NM
NM
NM
Previous RTh/CTh (%)
NM
NM
Median (range): 220 (120–340)
Median (range): 165 (90–240)
Median (IQR): 123.5 (116.2–141.6), p = 0.273
Median (IQR): 120 (102.7–135.7)
Mean (SD): 176 (29.4)
Mean (SD): 177.1 (62.7), p = 0.054
Operative time (in min)
Median (range): 34 (13–68)
Median (range): 32 (16–52)
Median (range): 29.5 (5–54)
Median (range): 19.5 (1–38)
Median (IQR): 12.0 (6.0–16.0), p = 0.782
Median (IQR): 12 (7–18)
NM
Mean (SD): 18.3 (9.4), p = 0.32
Nr of dissected LNs
Arch Gynecol Obstet
52
51
24
20
33
Pakish [25]
Zanagnolo [28]
Lambaudie [22]
Vizza [27]
Magrina [23]
1
5
8
Chon [16]
Jacob [21]
Fastrez [19]
Case reports
Nr of patients
References
Table 2 continued
IIIA: 3/52 (5.8), IIIC1: 3/52 (5.8),
Mixed: 12/52 (23.1), MMMT: 2/52 (3.9)
IB2: 16/24 (66.7),
Cervical SCC Cervical SCC Cervical SCC Cervical SCC Cervical SCC
78
61
41
66
52
Cervical SCC
Cervical adenocarcinoma
Endometrial cancer: 5/5 (100)
Cervical cancer
Peritoneal cancer: 1/33 (3)
Ovarian cancer: 20/33 (60), vaginal cancer: 2/33 (6),
Endometrial cancer: 6/33 (18),
Cervical cancer: 4/33 (12),
TIIBNxM0
TIIBNxM0
TIIIANxM0
TIIBNxM0
TIIBNxM0
TIVANxM0
TIB2N1M0
TIIBNxM0
NM
IIB
Ovarian cancer: IA–IIIB NM
Endometrial cancer: IC– IIIC
Endometrial cancer: 6/20 (30), Ovarian cancer: 12/20 (60)
Cervical cancer: IIB
Cervical cancer: 2/20 (10),
IIIB: 1/24 (4.2)
IIIA: 1/24 (4.2),
IIB: 6/24 (25),
Cervical cancer
Cervical cancer 24/24 (100)
Tubal cancer: 4/51 (7.8)
Cervical cancer: 1/51 (1.9),
NM
–
NM
RTh
NM
NM
NM
Median (range):137.5 (90–185)
Median (range): 213 (186–265)
120
Mean (range): 42 (19–64)
Mean (range): 224 (160–300)
Mean (SD): 163.7 (6)
Mean: 270
II: 3/52 (5.8),
Clear cell: 2/52 (3.9),
NM
IB: 7/52 (13.5),
UPSC: 4/52 (7.7),
Ovarian cancer: 40/51 (78.4), Endometrial cancer: 6/51 (11.7),
Median (range): 297.5 (182–633)
NM
IA: 33/52 (63.5),
Endometrioid: 32/52 (61.5),
IIIC2: 3/52 (5.8)
Operative time (in min)
Previous RTh/ CTh (%)
Clinical stage of primary neoplasia (%)
Histological type (%)
Cervical SCC
Mmedian (range): 24.3 (17.3–31.3)
Median (range): 25.2 (22.5–32.1)
32
Mean (range): 26.3 (22–38.9)
Median (range): 27.8 (21–35)
Mean (SD): 22 (3.4)
Mean (range): 23 (18–33)
Median (range): 30.2 (19.1–51.2)
BMI (in kg/m2)
38
49
44
Median (range): 67 (61–75)
59
Mean (range): 62 (25–79)
Median (range): 61.3 (34–73)
Mean (SD): 43.1 (8.8)
Mean (range): 41 (18–59)
Median (range): 62 (36–80)
Age of patient (in y.o.)
13
12
4
1
38
12
17
15
Mean (range): 8.2 (4–17)
1
Mean (range): 12.9 (2–27)
Mean (range): 12.5 (7–17)
Mean (SD): 13.3 (7.3)
Para-aortic: 14 (6)
Mean (SD): Pelvic: 15 (7),
Pelvic Median (range): 13.5 (1–36)
Median (range): 4.5 (1–18)
Para-aortic
Nr of dissected LNs
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123
123
Mean (SD): 126.6 (56.6)
39/97 (40.2)àà
NM
NM
James [39]
Coronado [17]
Fastrez [18]
NM
Median (IQR): 93.5 (68–120), p = 0.075
Median (IQR): 75 (46.3–97.5)
Mean (SD): 113.5 (132.8), p = 0.28
NM
NM
8/21 (38),àà p = 0.01
Mean (SD): 149.8 (118.8)
NM
EBL (in ml)
6/51 (11.7)àà
Nr of positive LNs
NM
Hudry [40]
Case series Akladios [41]
References
Table 2 continued
–
1/22 (4.5)
–
–
0/58, p = 0.39
4/429 (1)
3/21 (14.2)
1/51 (1.3)
Conversion to open (%)
Bowel injuries: 2/51 (4) Urinary injuries: 1/51 (2) Vessel injuries: 2/51 (4) Urinary injuries: 1/21 (4.8) Vessel injuries: 2/21 (9.5) Post-op: Lymphocyst: 25/429 (6) l Post-op: Lymphocyst: 7/58 (12)$$ Intra-op: 0/97 Post-op: Lymphedema: 5/97 (5.2), Transient ascites: 3/97 (3.1), Chylous ascites: 3/97 (3.1), Small bowel obstruction: 1/97 (1), Hematoma 1/97 (1), Port site cellulites; 1/97 (1), Wound seroma: 1/97 (1) Intra-op: IMA injury: 2/32 (6.25) Post-op: Severe diarrhea: 1/32 (3.1), Ureteral leak: 1/32 (3.1) Post-op: Ileus: 2/30 (6.7), Port-site haematoma: 1/30 (3.3), Hemoperitoneum: 1/30 (3.3) Intra-op: Aortic injury: 1/22 (4.5) Post-op: Lymphocele: 2/22 (9), Port site hernia: 1/22 (4.5) Post-op: Lymphocele: 1/8 (12.5)
Complications (intra-op or post-op) (%)
–
Median (range): 3 (2–4)
Median (range): 6 (2–10)
NM
Y: 1/22
Median (IQR): 2 (2–3)
Median (IQR): 2 (2–5.2), p = 0.161
NM
Y: 1/32
NM
Mean (SD): 2.7 (0.8), p = 0.001
Mean (SD): 3.5 (1.9)
Mean (range): 5.6 (2–14), p = 0.049
Mean (range): 7.7 (2–40)
Hospital stay (in days)
N
NM
NM
NM
NM
NM
Follow up (in mo)
–
Y: 10/487
Y: 1/5, p = 0.26
Y: 9/18
Transfusion (Y/N)
NM
NM
NM
NM
NM
NM
NM
Recurrence
Arch Gynecol Obstet
NM
NM
Mean (range): 1 (0–4)
Zanagnolo [28]
Lambaudie [22]
Vizza [27]
NM
Mean (SD): 154.6 (171)
Mean (range): 50 (20–200)
Median (range): 67.5 (20–1800)
NM
5/19 (26)àà
7/52 (13.5)
NM
4/16 (25)àà
Kimmig [38]
Pakish [25]
EBL (in ml)
Nr of positive LNs
References
Table 2 continued
–
–
–
2/52 (3.9)
–
–
Conversion to open (%) Post-op: Vein thrombosis: 1/16 (6), Post-op aphasia 1/16 (6) Post-op: Lymphocele: 2/19 (11), Post-op bleeding: 1/19 (5), Port site infection: 1/19 (5) Intra-op: Vascular injury: 1/52 (1.9) Post-op: Respiratory infection: 1/52 (1.9), Urinary: 1/52 (1.9), Port site infection: 1/52 (1.9), Haematoma/lymphocele: 2/52 (3.9), Renal/urinary complications: 2/52 (3.9) Intra-op: Bleeding: 1/51 (3.9) Post-op: Chylous ascites: 7/51 (13.7), Vaginal leakage 2/51 (3.9), Ureteral fistula: 1/51 (1.9), Femoral nerve injury: 1/51 (1.9), Legs edema: 4/51 (7.8), Port-site hernia: 2/61 (3.9), Lymphocele: 4/51 (7.8), Lymphatic ascites 1/51 (1.9) Post-op: Lymphocele: 1/24 (4.2) Intra-op: Iliac vein injury: 1/20 (5) Post-op: Chylous ascites: 1/5 (20)
Complications (intra-op or post-op) (%)
Mean (range): 10.4 (1–21.6)
N
Median (range): 26 (1–56)
Y: 3/51 (5.8)
NM
NM
Y: 4/52 (7.7)
N
Median (range): 20 (12–28)
Median (range): 22 (13–28)
Follow up (in mo)
Y: 2/19
Y: 1/16
Transfusion (Y/N)
Median (range): 2 (1–4)
Mean (SD): 3.1 (1.6)
Median (range): 3 (2–7.5)
Mean: 2
Median (range): 9 (6–33)
Median (range): 10 (5–25)
Hospital stay (in days)
NM
NM
6/51 (11.7)
NM
1/19 (5)
2/16 (13)
Recurrence
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123
123
Mean (range): 2.6 (0–11)
Magrina [23]
2 5 2
–
–
1/8 (12.5)
NM
NM
NM
Recurrence
$$
$
##
#
Retroperitoneal group
Transperitoneal group
Cervical cancer patients and positive lymph nodes had adjuvant platinum-based chemotherapy/radiotherapy
Endometrial cancer patients (stage FIGO III) had six cycles of adjuvant platinum-based chemotherapy
Robotic-assisted transperitoneal (inframesenteric) group
Robotic-assisted transperitoneal (infrarenal) group
Conventional laparoscopic group
Refers to patients with positive lymph nodes
Calculated in weeks
Lymphadenectomy as isolated procedure In overall, regarding the total complications, no differences were found between the two groups (p = 0.31)
§§§
§§
§
àà
à
USA United States of America, y.o. years old, BMI body mass index, Nr number, EBL estimated blood loss, N No, Y yes, IMA inferior mesenteric artery, RTh radiotherapy, CTh chemotherapy, mo months, NM not mentioned, IQR interquartile range, DVT deep venous thrombosis, SCC squamous cell cervical carcinoma, SD standard deviation, NS not significant, MMMT malignant mixed Mu¨llerian tumour, UPSC uterine papillary serous carcinoma, LN lymph node
4
–
4
5
NM
1
N
Median (range): 1 (1–2)
2
Mean (range): 2.5 (1–13)
Hospital stay (in days)
7
NM
NM Mean (range): 12.8 (8–20)
N
NM
Follow up (in mo)
N
N
Transfusion (Y/ N)
–
–
Trocar site hernia: 1/5 (20)
Chylous ascites: 1/5 (20),
Post-op:
–
Lymphocele: 1/33 (3)
Post-op:
Bleeding: 1/33 (3)
Aorta injury: 1/33 (3),
Intra-op:
Complications (intra-op or post-op) (%)
–
NM
–
–
1/33 (3)
Conversion to open (%)
2
–
Fastrez [19]
Median (range): 150 (50–550)
200
Mean: 45
EBL (in ml)
–
1
NM
Chon [16]
Jacob [21]
Case reports
Nr of positive LNs
References
Table 2 continued
Arch Gynecol Obstet
Arch Gynecol Obstet
Techniques Extraperitoneal approach The inspection of peritoneal cavity is necessary in order to proceed to extraperitoneal lymphadenectomy. Through an umbilical transperitoneal port (10 mm trocar), the peritoneal cavity is inspected with the purpose to detect any intra-peritoneal lesions. A 15 mm incision is made at the left side of superior iliac spine. Through this incision and with blunt dissection of the abdominal muscles, the parietal fascia is accessed without opening the peritoneal fascia. The extraperitoneal space is created through digital dissection, which expands from the anterior surface of the lateral psoas muscle to the common iliac artery. A blunt-tip balloon trocar (10–12 mm) is placed through the incision for the introduction of the camera. Also, through this port, CO2 is insufflated with a stable pressure of 15 mmHg. An assistant port (10 mm) is positioned 1 cm above the corner of the pubic hair with the task to move ureters and ovarian vessels and to remove the endobag with the dissected lymph nodes. In addition, two additional trocars (8 mm) are placed both distal (8–10 cm) and medial (8–10 cm) to the camera port (one of which under the lowest rib on the anterior axillary line, at the level of umbilicus). The Da Vinci robotic system is situated contralateral to the side of the ports. Through the 8-mm ports, an ultrasonic harmonic scalpel and a bipolar forceps can be used. Lymph nodes located at para-aortic and preaortic regions are approached at zero degree. First and foremost, the identification of important structures (e.g. the aorta and its bifurcation, the vena cava, the ureters, the ovarian vessels) is fundamental before proceeding to the lymph node dissection. Before the removal of the trocars, a hole is created at the peritoneum anteriorly and laterally of the ureter to the intra-peritoneal cavity with the intention to avoid lymphocele. A drain is inserted above the pubis symphysis into the retroperitoneal space through the assistant port (10 mm). All the port entrances are closed with interrupted resorbable sutures, while the skin with nylon suture. Transperitoneal approach The Da Vinci robotic system is suggested to be placed at the head of the patient, while the patient is positioned in Trendelenburg position. The camera port (12 mm) is inserted 4 cm suprapubically and 2 cm laterally of the midline. Two additional trocars (10 mm) are placed 10–12 cm laterally to the camera port, and a third port is placed 12 cm laterally of the umbilicus. Monopolar scissors and a bipolar grasper are inserted via the two 10-mm ports. An accessory port can be placed between the camera
port and one of the additional 10-mm trocars, through which a fenestrated grasper could be inserted in order to retract the duodenum ventrally. After the entrance into the peritoneal cavity, the peritoneum over the midportion of the right common iliac artery is dissected up to the aortic bifurcation. A part of peritoneum is gently elevated ventrally with the use of grasping forceps, avoiding the entry of small bowel into the surgical field. Once having identified the aorta and its bifurcation, as well as the vena cava and the ureters, then the dissection of lymph nodes can be performed by removing initially the para-aortic and the interaortic nodes. The dissection is performed with excision of the lymph nodes over the vena cava. For the inframesenteric left aortic nodes, the peritoneal incision should be extended downwards from the aortic bifurcation to the left common iliac artery. At this point, in order to increase the exposure of both the inframesenteric left aortic nodes and the left infrarenal nodes, the inferior mesenteric artery may be transacted (before the transection of the artery, the viability of sigmoid should always be checked by temporarily clamping the inferior mesenteric artery). The dissection may be proceeded up to the left ovarian vein and the upper side of the left renal vein which can be considered, respectively, the lateral and upper limits of left aortic lymphadenectomy.
Discussion Assessment of the retroperitoneal lymph nodes is considered to be the standard of care in patients with gynaecological cancer. DaVinci robot can assist in the easier performance of such a technically challenging operation. The transperitoneal approach is the most widely used as the majority of the gynaecological oncologists are well trained to perform it; however, the extraperitoneal approach is increasingly used by well-trained teams worldwide. Till now, there is no comparison of the two methods and our review is trying to clarify the advantages and disadvantages of each technique. The extraperitoneal approach in comparison to the standard transperitoneal one presents a number of potential advantages. Firstly, the approach to the retroperitoneal space offers the possibility to limit and tamponate possible leaks of either blood or urine, avoiding the direct contact of urine or blood with bowel that can cause ileus [29]. The possibility of either vascular or intestinal injury is also decreased. Moreover, avoiding the entry into the peritoneal cavity can minimize the post-operative adhesions and hernia complications [30]. The CO2 insufflated into the working space is of lower pressure (about 12 mm Hg lower) and quantity in relation to the transperitoneal
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technique. Thus, complications related to CO2 passage into peritoneal cavity, such as subcutaneous emphysema, pneumothorax or even vagus nerve irritation, are quite negligible at the extraperitoneal technique. Moreover, the extraperitoneal approach reduces the necessity of extreme Trendelenburg position due to the fact that the abdominal viscera are retracted by peritoneum, offering a clear view of the surgical field. This is crucial in obese or elderly patients with comorbidities [31]. In particular, the decreased inclination during Trendelenburg position reduces the negative impact on ventilation and the usually increased peak pressure in the group of obese patients. However, the extraperitoneal technique may also present a few drawbacks. The restricted working space can be a serious issue especially for the not-so-experienced surgeons. In comparison to the transperitoneal approach, the port placement is one of the reasons that the operative time is usually prolonged, which can be easily interpreted into higher operating-room costs [25]. Moreover, the establishment of the retroperitoneal space and the detachment of peritoneum may create tension on various structures, such as the vesicourethral anastomosis [29]. In case of peritoneum tear during the formation of the working space and CO2 diffusion into the peritoneal cavity, an extra 5-mm port should be placed in the upper abdomen, in order to maintain steady the already-created surgical field. Utilizing the extraperitoneal approach, there is always the risk of creating lymphocele in case of pelvic lymphadenectomy, a probability that is insignificant after a transperitoneal approach where the lymphatic fluid can be absorbed and recycled within the peritoneal cavity [25, 31]. On the other hand, the transperitoneal approach may also present several advantages and disadvantages. The extensive working field and the relative easy port placement as well as the minimal risk of lymphocele are some of the strong points of the transperitoneal approach [31]. When bilateral lymphadenectomy is performed, the transperitoneal technique seems to be more efficient in comparison to the extraperitoneal approach which can be technically more challenging. Alternately, the potential disadvantages of the technique could include the risk of bowel injury or accidental perforation, the risk of vascular injuries, the probability of ileus due to a blood or urine leak and the need of severe Trendelenburg positioning of the patient which may have deep impact especially on patients with cardiopulmonary problems and increased intraocular pressure [16, 32]. As the role of extraperitoneal approach is already better clarified in urological patients, lessons could be learnt from their experience. For example, the presence of unilateral masses less than 5 cm diameter is an indication for minimally invasive extraperitoneal lymphadenectomy, and thus both laparoscopic- and robotic-assisted techniques have
123
oncological outcomes comparable to open surgery especially in the hands of experts [33]. Moreover, lymphocele may develop, in patients with prostatic carcinoma, when there is an invasion of the seminal vesicles or in cases of large tumour volume. Nevertheless, the scrupulous clipping of the lymphatic vessels does not always prevent the postoperative lymphocele [34, 35]. In an attempt to avoid this particular eventuality, some authors have proposed the formation of a peritoneal window after the completion of extraperitoneal lymphadenectomy in order to reduce the probability of lymphocele [36]. Various limitations should be taken into consideration in the evaluation of the findings of this paper. Some could argue that the main surgical approach in ovarian cancer is open surgery; however, there is a role of minimal invasive lymphadenectomies especially in fertility sparing procedures, and for this reason we included ovarian cancer in our analysis. The small number of the included studies, especially at the extraperitoneal approach in combination with the limited total number of the patients included, demonstrating that the evidence on the extraperitoneal lymphadenectomy is still new, and the improvement in the learning curve might differ the results. Besides that fact, trials with superior methodological quality (randomized control trials) are crucial in order to clarify technical details in both extraperitoneal and transperitoneal approaches. For example, we faced difficulties in performing such an analysis due to the heterogeneity of surgical approach in different institutions and the lack of a definition of what lymphadenectomy means leading to a range of retrieved nodes from 1 to 54 indicating a wide range of modifications of ‘‘lymphadenectomy’’. More specifically, it is very difficult to clarify from the included studies what each group means as pelvic or para-aortic lymph node dissection and where pelvic lymph node dissection ends or where paraaortic lymph node dissection starts. For this reason, we suggest that future randomized controlled trials should clarify with detailed definitions the inclusion criteria and the systematic approach of pelvic and para-aortic lymph node dissection in order to achieve better comparability of the surgery. Last but not least, even though our literature search presents wide range, it could be considered relatively selective by posing as limits the exclusion of abstracts, letters to the editor, surveys, reviews and animal studies. The restriction regarding the written language decreases further the number of the potentially included studies.
Conclusion In conclusion, robotic technology introduced a new dynamic in various surgical fields. The application of robotic-assisted surgery in complex operations of
Arch Gynecol Obstet
gynaecological oncology facilitated the pelvic and paraaortic lymphadenectomy. A reliable definition of the ‘‘kind’’ of lymphadenectomy used in each study is the first step in order to reach safe conclusions. Nevertheless, the lack of comparative studies, especially the randomized ones, cannot help us draw any safe conclusion regarding both the clinical outcomes and the possible superiority of extraperitoneal and transperitoneal approaches. Compliance with ethical standards Conflict of interest The authors declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.
References 1. Prasad SM, Shalhav AL (2013) Comparative effectiveness of minimally invasive versus open lymphadenectomy in urological cancers. Curr Opin Urol 23:57–64 2. Creasman WT, Morrow CP, Bundy BN, Homesley HD, Graham JE, Heller PB (1987) Surgical pathologic spread patterns of endometrial cancer. A Gynecologic Oncology Group Study. Cancer 60:2035–2041 3. Kilgore LC, Partridge EE, Alvarez RD et al (1995) Adenocarcinoma of the endometrium: survival comparisons of patients with and without pelvic node sampling. Gynecol Oncol 56:29–33 4. Mariani A, Webb MJ, Galli L, Podratz KC (2000) Potential therapeutic role of para-aortic lymphadenectomy in node-positive endometrial cancer. Gynecol Oncol 76:348–356 5. Delgado G, Bundy B, Zaino R, Sevin BU, Creasman WT, Major F (1990) Prospective surgical-pathological study of disease-free interval in patients with stage IB squamous cell carcinoma of the cervix: a Gynecologic Oncology Group study. Gynecol Oncol 38:352–357 6. Tanaka Y, Sawada S, Murata T (1984) Relationship between lymph node metastases and prognosis in patients irradiated postoperatively for carcinoma of the uterine cervix. Acta Radiol Oncol 23:455–459 7. Tinga DJ, Timmer PR, Bouma J, Aalders JG (1990) Prognostic significance of single versus multiple lymph node metastases in cervical carcinoma stage IB. Gynecol Oncol 39:175–180 8. Shah M, Lewin SN, Deutsch I et al (2011) Therapeutic role of lymphadenectomy for cervical cancer. Cancer 117:310–317 9. Burghardt E, Girardi F, Lahousen M, Tamussino K, Stettner H (1991) Patterns of pelvic and paraaortic lymph node involvement in ovarian cancer. Gynecol Oncol 40:103–106 10. Kigawa J, Minagawa Y, Itamochi H, Kanamori Y, Ishihara H, Terakawa N (1994) Retroperitoneal lymphadenectomy, including the para-aortic nodes in patients with stage III ovarian cancer. Am J Clin Oncol 17:230–233 11. Panici PB, Maggioni A, Hacker N et al (2005) Systematic aortic and pelvic lymphadenectomy versus resection of bulky nodes only in optimally debulked advanced ovarian cancer: a randomized clinical trial. J Natl Cancer Inst 97:560–566 12. Spirtos NM, Gross GM, Freddo JL, Ballon SC (1995) Cytoreductive surgery in advanced epithelial cancer of the ovary: the impact of aortic and pelvic lymphadenectomy. Gynecol Oncol 56:345–352 13. Iavazzo C, Darlas FM, Gkegkes ID (2013) The role of robotics in ovarian transposition. Acta Inform Med 21:135–137 14. Iavazzo C, Gkegkes ID (2014) Robotic technology for pelvic exenteration in cases of cervical cancer. Int J Gynaecol Obstet 125:15–17
15. Bats AS, Mimouni M, Bensaid C et al (2014) Robotic extraperitoneal paraaortic lymphadenectomy in gynecological cancers: feasibility, safety, and short-term outcomes of isolated and combined procedures. Int J Gynecol Cancer 24:1486–1492 16. Chon HS, Bush WD, Kang CW, Hoffman M (2013) Roboticassisted resection of isolated paraaortic lymph node recurrence with right lateral decubitus position. J Robotic Surg 7:205–207 17. Coronado PJ, Fasero M, Magrina JF, Herraiz MA, Vidart JA (2014) Comparison of perioperative outcomes and cost between robotic-assisted and conventional laparoscopy for transperitoneal infrarenal para-aortic lymphadenectomy (TIPAL). J Minim Invasive Gynecol 21:674–681 18. Fastrez M, Goffin F, Vergote I et al (2013) Multi-center experience of robot-assisted laparoscopic para-aortic lymphadenectomy for staging of locally advanced cervical carcinoma. Acta Obstet Gynecol Scand 92:895–901 19. Fastrez M, Vandromme J, George P, Rozenberg S, Degueldre M (2009) Robot assisted laparoscopic transperitoneal para-aortic lymphadenectomy in the management of advanced cervical carcinoma. Eur J Obstet Gynecol Reprod Biol 147:226–229 20. Gorostidi M, Larreategui J, Bernal T et al (2014) Robotic retroperitoneal paraaortic lymphadenectomy at Donostia University Hospital. J Minim Invasive Gynecol 21:480–485 21. Jacob KA, Zanagnolo V, Magrina JF, Magtibay PM (2011) Robotic transperitoneal infrarenal aortic lymphadenectomy for gynecologic malignancy: a left lateral approach. J Laparoendosc Adv Surg Tech A 21:733–736 22. Lambaudie E, Narducci F, Leblanc E et al (2012) Robotically assisted laparoscopy for paraaortic lymphadenectomy: technical description and results of an initial experience. Surg Endosc 26:2430–2435 23. Magrina JF, Long JB, Kho RM, Giles DL, Montero RP, Magtibay PM (2010) Robotic transperitoneal infrarenal aortic lymphadenectomy: technique and results. Int J Gynecol Cancer 20:184–187 24. Narducci F, Lambaudie E, Houvenaeghel G, Collinet P, Leblanc E (2009) Early experience of robotic-assisted laparoscopy for extraperitoneal para-aortic lymphadenectomy up to the left renal vein. Gynecol Oncol 115:172–174 25. Pakish J, Soliman PT, Frumovitz M et al (2014) A comparison of extraperitoneal versus transperitoneal laparoscopic or robotic para-aortic lymphadenectomy for staging of endometrial carcinoma. Gynecol Oncol 132:366–371 26. Vergote I, Pouseele B, Van Gorp T et al (2008) Robotic retroperitoneal lower para-aortic lymphadenectomy in cervical carcinoma: first report on the technique used in 5 patients. Acta Obstet Gynecol Scand 87:783–787 27. Vizza E, Mancini E, Baiocco E et al (2012) Robotic transperitoneal aortic lymphadenectomy in gynecologic cancer: a new robotic surgical technique and review of the literature. Ann Surg Oncol 19:3832–3838 28. Zanagnolo V, Rollo D, Tomaselli T et al (2013) Robotic-assisted transperitoneal aortic lymphadenectomy as part of staging procedure for gynaecological malignancies: single institution experience. Obstet Gynecol Int 2013:931318 29. Madi R, Daignault S, Wood DP (2007) Extraperitoneal v intraperitoneal robotic prostatectomy: analysis of operative outcomes. J Endourol 21:1553–1557 30. Huang M, Slomovitz BM, Ramirez PT (2009) Transperitoneal versus extraperitoneal para-aortic lymphadenectomy in patients with cervical cancer. Rev Obstet Gynecol 2:101–106 31. Atug F, Castle EP, Woods M, Srivastav SK, Thomas R, Davis R (2006) Transperitoneal versus extraperitoneal robotic-assisted radical prostatectomy: is one better than the other? Urology 68:1077–1081
123
Arch Gynecol Obstet 32. Gkegkes ID, Karydis A, Tyritzis SI, Iavazzo C (2014) Ocular complications in robotic surgery. Int J Med Robot 33. Kunit T, Janetschek G (2014) Laparoscopic and robotic postchemotherapy retroperitoneal lymph node dissection. Curr Opin Urol 24:162–167 34. Ghazi A, Scosyrev E, Patel H, Messing EM, Joseph JV (2013) Complications associated with extraperitoneal robot-assisted radical prostatectomy using the standardized Martin classification. Urology 81:324–331 35. Lee JY, Diaz RR, Cho KS et al (2013) Lymphocele after extraperitoneal robot-assisted radical prostatectomy: a propensity score-matching study. Int J Urol 20:1169–1176 36. Stolzenburg JU, Wasserscheid J, Rabenalt R et al (2008) Reduction in incidence of lymphocele following extraperitoneal radical prostatectomy and pelvic lymph node dissection by bilateral peritoneal fenestration. World J Urol 26:581–586 37. Wimberger P, Lehmann N, Kimmig R, Burges A, Meier W, Du Bois A (2007) Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group. Prognostic factors for complete debulking in advanced ovarian cancer and its impact on survival. An exploratory analysis of a prospectively randomized phase III study of the Arbeitsgemeinschaft Gynaekologische Onkologie
123
38.
39.
40.
41.
Ovarian Cancer Study Group (AGO-OVAR). Gynecol Oncol 106:69–74 Kimmig R, Iannaccone A, Buderath P, Aktas B, Wimberger P, Heubner M (2013) Definition of compartment based radical surgery in uterine cancer-part I: therapeutic pelvic and periaortic lymphadenectomy by Michael ho¨ckel translated to robotic surgery. ISRN Obstet Gynecol 25:1–17 James JA, Rakowski JA, Jeppson CN, Stavitzski NM, Ahmad S, Holloway RW (2015) Robotic transperitoneal infra-renal aortic lymphadenectomy in early-stage endometrial cancer. Gynecol Oncol 136:285–292 Hudry D, Ahmad S, Zanagnolo V, Narducci F, Fastrez M, Ponce J, Tucher E, Le´curu F, Conri V, Leguevaque P, Goffin F, Holloway RW (2015) Lambaudie E; SERGS Group. Robotically assisted para-aortic lymphadenectomy: surgical results: a cohort study of 487 patients. Int J Gynecol Cancer 25:504–511 Akladios C, Ronzino V, Schrot-Sanyan S, Afors K, Fernandes R, Baldauf JJ, Wattiez A (2015) Comparison between transperitoneal and extraperitoneal laparoscopic paraaortic lymphadenectomy in gynecologic malignancies. J Minim Invasive Gynecol 22:268–274
REVIEW
Robotic retroperitoneal lymph node dissection in gynaecological neoplasms: comparison of extraperitoneal and transperitoneal lymphadenectomy Christos Iavazzo1,2 • Ioannis D. Gkegkes3
Received: 17 March 2015 / Accepted: 3 July 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Objective The main aim of our study is to review the till now available literature data on the role of robotic retroperitoneal lymph node dissection in gynaecological cancers by comparing the extraperitoneal versus the transperitoneal approach. Methods A thorough and systematic search was performed in electronic databases of PubMed and Scopus. Results The extraperitoneal approach is described in 148 patients. The age of the patients ranged from 26 to 78 years. The indications included cervical, endometrial and ovarian carcinoma in 113, 22 and 12 patients, respectively. The operative time ranged between 45 and 410 min. The number of dissected lymph nodes ranged from 3 to 25, while only 13 of them were found to be positive. The mean estimated blood loss during the operation was 77 ml (range \50–200 ml). Seven cases were converted to open. The duration of hospital stay ranged from 2 to 14 days. The transperitoneal approach is described in 898 patients. The age of the patients ranged from 15 to 89 years. Cervical, endometrial and ovarian carcinomas were the principal neoplasias present in 248, 449 and 164 patients, respectively. The operative time ranged from 19 to 633 min. The number of dissected lymph nodes ranged from 1 to 54, while the total number of patients with positive lymph nodes dissected was 56 & Christos Iavazzo [email protected] 1
Gynaecological Oncology Department, Christie Hospital, Manchester, UK
2
38, Seizani Str., Nea Ionia, 14231 Athens, Greece
3
First Department of Surgery, General Hospital of Attica ‘‘KAT’’, Athens, Greece
patients. The estimated blood loss during the operation varied between 20 and 1800 ml. Only 9 out of 898 patients were converted to open. The duration of hospital stay ranged from 1 to 40 days. Conclusion A reliable definition of the ‘‘kind’’ of lymphadenectomy used in each study is the first step in order to reach safe conclusions. The lack of comparative studies, especially the randomized ones, cannot help us draw any safe conclusion regarding both the clinical outcomes and the possibility of any superiority of these different approaches (extraperitoneal and transperitoneal). Keywords Robotics Lymphadenectomy Retroperitoneal Extraperitoneal Transperitoneal Gynaecological cancer
Introduction The main role of lymph node dissection is to decrease or even better eradicate the risk of recurrence [1]. Furthermore, lymph node dissection may also provide more information about disease staging or it may lead to the early recognition of lymph node metastases, offering the opportunity to the patient to start earlier the adjuvant therapy. The lymphadenectomy in gynaecological malignancies is controversial, and several studies are ongoing to answer the question of should we or should we not dissect systematically the lymph nodes in cancers as endometrium or ovarian cancer. More specifically, the Gynecologic Oncology Group (GOG)—Protocol 33 showed that patients with endometrial cancer can have extra-uterine disease in 22 % of the cases including disease spread to pelvic lymph nodes in 9 % and para-aortic lymph nodes in 5 % [2]. For this reason, the International
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Federation of Gynecology and Obstetrics (FIGO) included pelvic and para-aortic lymph node status in the surgical staging system for endometrial cancer. It is shown that the performance of pelvic and para-aortic lymph node dissection can lead to diagnostic and therapeutic advantages [3, 4]. However, lymph node dissection as a part of endometrial cancer staging, especially in low-risk patients, is still controversial. Regarding cervical cancer, the status of pelvic and para-aortic lymph nodes is one of the most important prognostic factors which also affects the extent of the radiation field [5–7]. GOG study showed that the 3-year disease-free interval was 74 % for those with positive nodes versus 86 % for node-negative patients with stage IB cervical cancer [5]. It is accepted that a more thorough lymph node dissection could increase the likelihood of detecting occult metastatic disease. Recently, Shah et al. showed that the extent of lymph node dissection in women with early-stage cervical cancer influences survival as node-negative patients have better survival when a greater number of lymph nodes are dissected [8]. In ovarian cancer patients, the role of lymph node dissection has been debated. Retroperitoneal lymph node involvement occurs in 5–25 and 50–80 % of women with early and advanced ovarian cancer, respectively. Retrospective studies showed that lymph node dissection is associated with an improvement of staging, complete cytoreduction and a survival benefit, even though current ongoing prospective trial on ovarian cancer (LION study) will help give a definitive answer on this issue and investigate if these data—especially the node ratio—have therapeutic implications and may be considered in future staging [9–12, 37]. Minimally invasive techniques have become the gold standard of care as they decrease morbidity, hospital stay and period of return to normal activity. They have also been used for retroperitoneal lymph node dissection with comparable outcomes regarding the number of lymph nodes and prognosis. The majority of the cases are performed with the transperitoneal approach; however, recently extraperitoneal approach has been widely used. Robotic technology is characterized by the three-dimensional view, the infiltration of surgeon’s natural tremor, the improved dexterity and less operator fatigue, and for this reason the important role that a robotic approach can have in the lymph node dissection is highlighted [13, 14]. The main aim of our study is to review the till now available literature data on the role of robotic technique in extraperitoneal and transperitoneal lymph node dissection of patients with gynaecological cancers.
123
Methods Data sources A thorough and systematic search was performed in electronic databases of PubMed (28 April 2015) and Scopus (28 April 2015). The search strategy adopted at the aforementioned databases was based on a combination of keywords: (robot OR robotic OR telesurgery) AND (retroperitoneal OR transperitoneal OR extraperitoneal) AND (lymphadenectomy OR lymph node dissection). The references of the included articles were also searched for additional studies. Study selection criteria In this review, all the studies that reported data relevant on the role of robotics in both extraperitoneal and transperitoneal lymph node dissection were included. Abstracts from conferences, letters to the editor, surveys, review articles and animal studies were not included in the analysis. Papers published in other languages than English, Spanish, German, French, Italian or Greek were excluded.
Results A total of 107 and 540 search results were retrieved during the performed search in PubMed and Scopus databases, respectively, among of which 18 studies were identified as eligible for inclusion in our review [15–28, 39–41]. One additional study was identified through hand-searching of references [38]. In Fig. 1, the included studies are represented graphically (flow diagram). The major characteristics of the included studies in our review (number of patients included, age of patients, patients’ body mass index, histological type of tumour, clinical stage of the primary cancer, history of previous radiotherapy/chemotherapy, duration of operative time, number of dissected lymph nodes, number of positive lymph nodes, estimated blood loss during lymph node dissection, cases of conversion to open, complications (intra- or post-operative), intra-operative need of transfusion, duration of hospital stay, duration of follow-up and the presence of recurrence during follow-up) are presented in Tables 1 and 2. Regarding the extraperitoneal lymphadenectomy, the literature search revealed 6 case series and 2 case reports. In total, 148 patients were included in our review. The age of the patients ranged from 26 to 78 years. The body mass
Arch Gynecol Obstet Fig. 1 Flow diagram that presents in detail the selection process of the included articles in our review
index (BMI) of the patients ranged from 19 to 48.83 kg/m2. Cervical, endometrial and ovarian carcinomas were present in 113, 22 and 12 patients, respectively. A history of radiotherapy and a combination of radio/chemotherapy was present in 2 and 2, respectively. The majority of the included carcinomas were of low clinical stage. Specifically, in cases of cervical carcinoma, the greatest part of the patients was up to stage IIB (59 out of 113), while 33 out of 113 patients presented a clinical stage superior to IIB. The major part of the patients with endometrial cancer was inferior to stage III (7 out of 22). The main clinical stage of the patients with ovarian carcinoma was stage I (2 out of 12). The operative time ranged between 45 and 410 min. The number of dissected lymph nodes ranged from 3 to 25, while only 13 of them were found to be positive to neoplasia. The mean estimated blood loss during the operation was 77 ml (range \50–200 ml). Seven cases of conversion to open were reported due to poor visibility (1 out of 7), loss of the pneumo-retroperitoneum (1 out of 7), injury of the left ureter (1 out of 7), major bleeding (2 out of 7), enlarged uterus (1 out of 7) and the need to perform Bricker procedure (1 out of 7). Among the intra-operative complications, ureteral injury, vascular injury and pneumothorax were found in 3, 4 and 1 patients, respectively. Regarding the post-operative complications, seven cases of lymphocysts, one case of digestive fistula, one case of plexus brachial paralysis, one case of pulmonary embolism, one case of surgical site infection, one case of urinoma, two cases of haematoma and two cases of lymphocele were reported. The necessity of transfusion was present only in two patients without any reference to the quantity of the blood loss. The duration of hospital stay ranged from 2 to 14 days. None of the included patients presented disease recurrence during the follow-up period which was not mentioned in none of the included studies.
Regarding the most widely used transperitoneal lymphadenectomy, the utilized search strategy revealed 11 case series and 3 case reports. In our review, 898 patients were included. The age of the patients ranged from 15 to 89 years. The BMI of the patients ranged from 16 to 57 kg/m2. Cervical, endometrial and ovarian carcinomas were the principal neoplasias present in 248, 449 and 164 patients, respectively. A history of radiotherapy, chemotherapy and a combination of radio/chemotherapy was present in 3, 8 and 7 patients, respectively. The majority of the included carcinomas were of low clinical stage. In particular, in cases of cervical carcinoma, the large part of the patients was of stage IB2 (114 out of 248), while the major part of patients with endometrial cancer was inferior of stage II. The clinical stage of the patients with ovarian carcinoma ranged between stage IA and IIIB (72 out of 164). The operative time ranged from 19 to 633 min. The number of dissected lymph nodes ranged from 1 to 54, while the total number of patients with positive lymph nodes dissected was 56. The estimated blood loss during the operation varied between 20 and 1800 ml. Only in 9 out of 898 patients, the conversion to open was reported because of vascular injury (5 out of 9), bowel injury (2 out of 9) and poor visibility (2 out of 9). The most common intra-operative complications were vascular injuries and bleeding present in 8 and 2 patients, respectively. The most common post-operative complications included lymphocysts, lymphocele, chylous ascites, port-site hernia and haematoma, which were found in 25, 13, 10, 4 and 3 patients, respectively. Transfusion was required in 31 patients (for blood loss over 500 ml). The duration of hospital stay ranged from 1 to 40 days. The follow-up period ranged between 1 and 56 months. Disease recurrence during follow-up was found only in 10 patients.
123
123
Hudry [40]
Akladios [41]
Case series
References
Mean (range): 26.6 (16.2–50) Mean (range): 22.5 (16.63–35)$
Mean (range): 58 (15–89)
Mean (range): 49 (23–79)$
429#
Mean (range): 26.9 (19–48), p = 0.09
Mean (range): 55.2 (38–75), p = 0.53
21##
Mean (range): 23.5 (16–35)
BMI (in kg/m2)
Mean (range): 53.3 (19–78)
Age of patient (in y.o.)
51#
Nr of patients
Other: 9/429 (2)
Cervical cancer: 107/429 (25)
Ovarian/tubal cancer: 60/429 (14),
Endometrial cancer: 253/429 (59),
Cervical cancer: 16/21 (76.3), p = 0.028
Ovarian cancer: 3/21 (14.3),
Endometrial cancer: 1/21 (4.8),
Unknown: 2/429 (0.5)
IVA: 3/429 (1)
IIIB: 4/429 (1)
IIIA: 4/429 (1)
IIB: 39/429 (9)
IIA: 4/429 (1)
IB1: 32/429 (7.5) IB2: 17/429 (4)
IA2: 1/429 (0.5)
Cervical cancer: IA1: 1/429 (0.5)
IV: 4/429 (1)
IIIC: 32/429 (7.5)
IIIA: 23/429 (5.4)
II: 18/429 (4)
IB: 115/429 (27)
Endometrial cancer: IA: 59/429 (14)
NM
NM
RTh/CTh: 2/21 (9.5)
CTh: 0/21
RTh: 2/21 (9.5)
RTh/CTh: 7/51 (14)
Cervical cancer: 22/51 (44)
RTh: 2/51 (4)
Previous RTh/CTh (%)
CTh: 8/51 (16)
NM
Clinical stage of primary neoplasia (%)
Ovarian cancer: 20/51 (40),
Endometrial cancer: 8/51 (16),
Histological type (%)
Table 1 Studies reporting data regarding the robot-assisted retroperitoneal lymph node dissection
Mean (SD): 200.4 (66)
Mean (range): 125.7 (45–180), p = 0.001
Mean (range): 200.2 (35–360)
Operative time (in min)
Mean (SD): 16.6 (8.9)
Mean (range): 13 (3–25), p = 0.015
Mean (range): 17 (4–37)
Nr of dissected LNs
Arch Gynecol Obstet
Bats [15]
References
Median (IQR): 55 (42–64)
Median (IQR): 24.1 (20.9–26.1)
Mean (range): 25 (19–48.83)$
Mean (range): 52 (27–74)$
24
Mean (range): 26.6 (20.82–33.2)
Mean (range): 62 (26–74)
58##
BMI (in kg/m2)
Age of patient (in y.o.)
Nr of patients
Table 1 continued
IIIB: 1/25 (4)
IC: 1/25 (4)
Ovarian cancers:
IIIC: 2/25 (8)
II: 1/25 (4)
IB: 2/25 (8)
IVA: 1/25 (4) Endometrial cancers: IA: 2/25 (8)
IIIB: 1/25 (4)
IIIA: 1/25 (4)
IIB: 5/25 (20)
IIA: 2/25 (8)
IB2: 2/25 (8)
Endometrial carcinoma: 8/25 (32) Ovarian carcinoma: 2/25 (8)*
Cervical cancers: IB1: 1/25 (4)
IVA: 2/58 (3.5)
IIIB: 2/58 (3.5)
IIIA: 5/58 (1)
IIA: 6/58 (1.4) IIB: 27/58 (47)
IB2: 8/58 (2)
IB1: 1/58 (1.7)
Cervical cancer:
Unknown: 2/58 (3.5)
IV: 4/58 (7)
IIIC: 2/58 (3.5)
Endometrial cancer: IA: 2/58 (3.5)
Clinical stage of primary neoplasia (%)
Cervical carcinoma: 15/25 (60)
Cervical cancer: 50/58 (86)
Ovarian/tubal cancer: 4/58 (7),
Endometrial cancer: 4/58 (7),
Histological type (%)
–
NM
Previous RTh/CTh (%)
Median (IQR): 240 (180–300)
Mean (SD): 177.1 (62.7), p = 0.054
Operative time (in min)
Median (range): 18 (14–25)
Mean (SD): 18.3 (9.4), p = 0.32
Nr of dissected LNs
Arch Gynecol Obstet
123
123
13
7
15
Gorostidi [20]
Fastrez [18]
Lambaudie [22]
5
5
Narducci [24]
Vergote [26]
Case reports
Nr of patients
References
Table 1 continued
21.5 28.8 25.2
45
74
62
25
56 24.4
25
49
40
29
65
19.3
23
27
24
61
Mean (SD): 27.4 (5.16)
Median (range): 24 (19–29)
Median (range): 31.9 (20–41.5)
BMI (in kg/m2)
28
Mean (SD): 49 (11.3)
Median (range): 50.5 (27–74)
Median (range): 60.3 (42–78)
Age of patient (in y.o.)
IIB: 1/13 (7.7)
Endometrial carcinoma: 9/13 (69.2)
IIA: 1/15 (6.7) IIB: 5/15 (33.3) IIIA: 1/15 (6.7)
Ovarian/tubal cancer 1/15 (6.7) Lymph node recurrence: 1/15 (6.7)
Cervical SCC
Cervical SCC
IIB
IIIB
IIB
IIB
IIB
NM
NM
NM
IIB
NM
73
60
65
82
139
130
215
165
235
240
IB2: 6/15 (40),
–
Mean (SD): 202.1 (64)
NM
Cervical cancer
Cervical cancer 13/15 (86.7)
IIB
Median (range): 100 (60–140)
NM
Cervical carcinoma
[IB2
IA: 1/13 (7.7)
Ovarian carcinoma:
IB: 1/13 (7.7)
IA: 8/13 (61.5)
Endometrial carcinoma:
IIIB: 1/13 (7.7)
Mean (range): 323 (180–410)
NR
Cervical carcinoma:
Cervical carcinoma: 2/13 (15.4)
Ovarian carcinoma: 2/13 (15.4)
Operative time (in min)
Previous RTh/CTh (%)
Clinical stage of primary neoplasia (%)
Histological type (%)
12
9
7
9
9
12
20
17
11
9
Mean (SD): 16.7 (8)
Median (range): 9.5 (7–12)
Median (range): 12 (4–21)
Nr of dissected LNs
Arch Gynecol Obstet
NM
NM
Fastrez [18]
Lambaudie [22]
Case reports
–
Gorostidi [20]
Mean (SD): 70.9 (69.3)
NM
NM
NM
Mean (SD): 113.5 (132.8), p = 0.28
NM
NM
Mean (SD): 149.8 (118.8)
NM
8/21 (38), p = 0.01
NM
NM
EBL (in ml)
6/52 (11.6)
Nr of positive LNs
Bats [15]
Hudry [40]
Akladios [41]
Case series
References
Table 1 continued
–
–
1
3
0/58, p = 0.39
4/429 (1)
3/21 (14.2)
1/51 (1.3)
Conversion to open
Haematoma: 1/15 (6.7)
Post-op:
Ureteral injury: 1/7 (14.3)
Intra-op:
Lymphocele: 1/13 (7.7)
Urinoma: 1/13 (7.7)
SSI: 1/13 (7.7)
Post-op:
IMA rupture: 1/13 (7.7)
Intra-op:
Lymphocele: 1/24 (4) Pulmonary embolism: 1/24 (4)
Blood transfusion: 1/24 (4)
Plexus brachial paralysis: 1/24 (4)
Digestive fistula: 1/24 (4)
Post-op:
Transaction of renal lower pole artery: 1/24 (4)
Bilateral PNX: 1/24 (4)
Intra-op:
Lymphocyst: 7/58 (12)$$
l Post-op:
Post-op: Lymphocyst: 25/429 (6)
Vessel injuries: 2/21 (9.5)
Urinary injuries: 1/21 (4.8)
Vessel injuries: 2/51 (4)
Urinary injuries: 1/51 (2)
Bowel injuries: 2/51 (4)
Complications (intra-op or post-op) (%)
N
N
Y: 1/13
N
Y: 10/487
Y: 1/5, p = 0.26
Y: 9/18
Transfusion (Y/N)
NM
NM
NM
NM
NM
NM
NM
NM
Follow up (in mo)
Mean (SD): 2.6 (0.6)
Median (range): 2.5 (2–3)
Mean: 3.4
Median (IQR): 5 (4–8)
Mean (SD): 2.7 (0.8), p = 0.001
Mean (SD): 3.5 (1.9)
Mean (range): 5.6 (2–14), p = 0.049
Mean (range): 7.7 (2–40)
Hospital stay (in days)
NM
NM
NM
NM
NM
NM
NM
NM
Recurrence
Arch Gynecol Obstet
123
123 50 50 50 50 50
5 –
–
–
–
Vergote [26]
–
–
–
Ureteral injury:
– Intra-op:
– N
N
Transfusion (Y/ N)
NM
NM
Follow up (in mo)
2
2
2
2 3
NM
Hospital stay (in days)
NM
NM
Recurrence
$$
$
##
#
*
In overall, regarding the total complications, no differences were found between the two groups (p = 0.31)
Lymphadenectomy as isolated procedure
Retroperitoneal group
One patient had both endometrial and ovarian cancers Transperitoneal group
USA United States of America, y.o. years old, BMI body mass index, Nr number, EBL estimated blood loss, N No, Y yes, IMA inferior mesenteric artery, RTh radiotherapy, CTh chemotherapy, mo months, NM not mentioned, SCC squamous cell carcinoma, LN lymph node, SSI surgical site infection, IQR interquartile range, PNX pneumothorax
–
Post-op: Lymphocele, seroma/haematoma
–
50 \50
–
–
Complications (intra-op or post-op) (%)
50
–
Conversion to open
180
200
–
Narducci [24]
EBL (in ml)
Nr of positive LNs
References
Table 1 continued
Arch Gynecol Obstet
Hudry [40]
Akladios [41]
Case series
References
Mean (range): 26.6 (16.2–50) Mean (range): 22.5 (16.63–35)$
Mean (range): 55.2 (38–75), p = 0.53
Mean (range): 58 (15–89)
Mean (range): 49 (23–79)$
21##
429#
Mean (range): 26.9 (19–48), p = 0.09
Mean (range): 53.3 (19–78)
Mean (range): 23.5 (16–35)
Age of patient (in y.o.) BMI (in kg/m2)
51#
Nr of patients
Other: 9/429 (2)
Cervical cancer: 107/429 (25)
Ovarian/tubal cancer: 60/429 (14),
Endometrial cancer: 253/429 (59),
Cervical cancer: 16/21 (76.3), p = 0.028
Ovarian cancer: 3/21 (14.3),
Endometrial cancer: 1/21 (4.8),
Cervical cancer: 22/51 (44)
Ovarian cancer: 20/51 (40),
Endometrial cancer: 8/51 (16),
Histological type (%)
Table 2 Studies reporting data regarding the robot-assisted transperitoneal lymph node dissection
Unknown: 2/429 (0.5)
IVA: 3/429 (1)
IIIB: 4/429 (1)
IIIA: 4/429 (1)
IIB: 39/429 (9)
IIA: 4/429 (1)
IB1: 32/429 (7.5) IB2: 17/429 (4)
IA2: 1/429 (0.5)
Cervical cancer: IA1: 1/429 (0.5)
IV: 4/429 (1)
IIIC: 32/429 (7.5)
IIIA: 23/429 (5.4)
II: 18/429 (4)
IB: 115/429 (27)
Endometrial cancer: IA: 59/429 (14)
NM
NM
Clinical stage of primary neoplasia (%)
NM
RTh/CTh: 2/21 (9.5)
CTh: 0/21
RTh: 2/21 (9.5)
RTh/CTh: 7/51 (14)
CTh: 8/51 (16)
RTh: 2/51 (4)
Previous RTh/CTh (%)
Mean (SD): 200.4 (66)
Mean (range): 125.7 (45–180), p = 0.001
Mean (range): 200.2 (35–360)
Operative time (in min)
Mean (SD): 16.6 (8.9)
Mean (range): 13 (3–25), p = 0.015
Mean (range): 17 (4–37)
Nr of dissected LNs
Arch Gynecol Obstet
123
123
Kimmig [38]
Median (range): 46 (31–71)
19
Median (range): 54.5 (36–73)
8§
Median (range): 59 (26–78)
Median (range): 55 (32–78)
22
16
Median (IQR): 59 (38.6–66.3), p = 0.408
30
Fastrez [18]
Median (IQR): 57.5 (47.5–66.7)
32
Coronado [17]
Mean (SD): 65.6 (11.3)
Median (range): 23 (18–33)
Median (range): 32 (20–57)
Median (range): 24.5 (17–32)
Median (range): 27 (17–37)
Median (IQR): 25 (21.6–27.1), p = 0.193
Median (IQR): 25.4 (21.6–30.4)
Mean (SD): 31.9 (7.1)
Mean (range): 25 (19–48.83)$
Mean (range): 52 (27–74)$
97
Mean (range): 26.6 (20.82–33.2)
Mean (range): 62 (26–74)
58##
BMI (in kg/m2)
Age of patient (in y.o.)
Nr of patients
James [39]
References
Table 2 continued
Cervical carcer
Endometrial cancer:
Cervical carcer
Cervical cancer: 30/62 (48.4)
Ovarian cancer: 12/62 (19.4),
Endometrial cancer: 20/62 (32.2),
Endometrial cancer
Cervical cancer: 50/58 (86)
Ovarian/tubal cancer: 4/58 (7),
Endometrial cancer: 4/58 (7),
Histological type (%)
II: 1/19 (5)
I: 18/19 (95)
III: 3/16 (9)
I: 13/16 (81)
[IB2
NM
IIIC2: 18/97 (18.6)
IIIC1: 21/97 (21.7)
IIIB: 1/97 (1)
IIIA: 1/97 (1)
IB: 17/97 (17.5) II: 4/97 (4.1)
IA: 35/97 (36.1)
IVA: 2/58 (3.5)
IIIB: 2/58 (3.5)
IIIA: 5/58 (1)
IIB: 27/58 (47)
IIA: 6/58 (1.4)
IB2: 8/58 (2)
IB1: 1/58 (1.7)
Cervical cancer:
Unknown: 2/58 (3.5)
IV: 4/58 (7)
IIIC: 2/58 (3.5)
Endometrial cancer: IA: 2/58 (3.5)
Clinical stage of primary neoplasia (%)
NM§§§
NM§§
NM
NM
NM
NM
Previous RTh/CTh (%)
NM
NM
Median (range): 220 (120–340)
Median (range): 165 (90–240)
Median (IQR): 123.5 (116.2–141.6), p = 0.273
Median (IQR): 120 (102.7–135.7)
Mean (SD): 176 (29.4)
Mean (SD): 177.1 (62.7), p = 0.054
Operative time (in min)
Median (range): 34 (13–68)
Median (range): 32 (16–52)
Median (range): 29.5 (5–54)
Median (range): 19.5 (1–38)
Median (IQR): 12.0 (6.0–16.0), p = 0.782
Median (IQR): 12 (7–18)
NM
Mean (SD): 18.3 (9.4), p = 0.32
Nr of dissected LNs
Arch Gynecol Obstet
52
51
24
20
33
Pakish [25]
Zanagnolo [28]
Lambaudie [22]
Vizza [27]
Magrina [23]
1
5
8
Chon [16]
Jacob [21]
Fastrez [19]
Case reports
Nr of patients
References
Table 2 continued
IIIA: 3/52 (5.8), IIIC1: 3/52 (5.8),
Mixed: 12/52 (23.1), MMMT: 2/52 (3.9)
IB2: 16/24 (66.7),
Cervical SCC Cervical SCC Cervical SCC Cervical SCC Cervical SCC
78
61
41
66
52
Cervical SCC
Cervical adenocarcinoma
Endometrial cancer: 5/5 (100)
Cervical cancer
Peritoneal cancer: 1/33 (3)
Ovarian cancer: 20/33 (60), vaginal cancer: 2/33 (6),
Endometrial cancer: 6/33 (18),
Cervical cancer: 4/33 (12),
TIIBNxM0
TIIBNxM0
TIIIANxM0
TIIBNxM0
TIIBNxM0
TIVANxM0
TIB2N1M0
TIIBNxM0
NM
IIB
Ovarian cancer: IA–IIIB NM
Endometrial cancer: IC– IIIC
Endometrial cancer: 6/20 (30), Ovarian cancer: 12/20 (60)
Cervical cancer: IIB
Cervical cancer: 2/20 (10),
IIIB: 1/24 (4.2)
IIIA: 1/24 (4.2),
IIB: 6/24 (25),
Cervical cancer
Cervical cancer 24/24 (100)
Tubal cancer: 4/51 (7.8)
Cervical cancer: 1/51 (1.9),
NM
–
NM
RTh
NM
NM
NM
Median (range):137.5 (90–185)
Median (range): 213 (186–265)
120
Mean (range): 42 (19–64)
Mean (range): 224 (160–300)
Mean (SD): 163.7 (6)
Mean: 270
II: 3/52 (5.8),
Clear cell: 2/52 (3.9),
NM
IB: 7/52 (13.5),
UPSC: 4/52 (7.7),
Ovarian cancer: 40/51 (78.4), Endometrial cancer: 6/51 (11.7),
Median (range): 297.5 (182–633)
NM
IA: 33/52 (63.5),
Endometrioid: 32/52 (61.5),
IIIC2: 3/52 (5.8)
Operative time (in min)
Previous RTh/ CTh (%)
Clinical stage of primary neoplasia (%)
Histological type (%)
Cervical SCC
Mmedian (range): 24.3 (17.3–31.3)
Median (range): 25.2 (22.5–32.1)
32
Mean (range): 26.3 (22–38.9)
Median (range): 27.8 (21–35)
Mean (SD): 22 (3.4)
Mean (range): 23 (18–33)
Median (range): 30.2 (19.1–51.2)
BMI (in kg/m2)
38
49
44
Median (range): 67 (61–75)
59
Mean (range): 62 (25–79)
Median (range): 61.3 (34–73)
Mean (SD): 43.1 (8.8)
Mean (range): 41 (18–59)
Median (range): 62 (36–80)
Age of patient (in y.o.)
13
12
4
1
38
12
17
15
Mean (range): 8.2 (4–17)
1
Mean (range): 12.9 (2–27)
Mean (range): 12.5 (7–17)
Mean (SD): 13.3 (7.3)
Para-aortic: 14 (6)
Mean (SD): Pelvic: 15 (7),
Pelvic Median (range): 13.5 (1–36)
Median (range): 4.5 (1–18)
Para-aortic
Nr of dissected LNs
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123
123
Mean (SD): 126.6 (56.6)
39/97 (40.2)àà
NM
NM
James [39]
Coronado [17]
Fastrez [18]
NM
Median (IQR): 93.5 (68–120), p = 0.075
Median (IQR): 75 (46.3–97.5)
Mean (SD): 113.5 (132.8), p = 0.28
NM
NM
8/21 (38),àà p = 0.01
Mean (SD): 149.8 (118.8)
NM
EBL (in ml)
6/51 (11.7)àà
Nr of positive LNs
NM
Hudry [40]
Case series Akladios [41]
References
Table 2 continued
–
1/22 (4.5)
–
–
0/58, p = 0.39
4/429 (1)
3/21 (14.2)
1/51 (1.3)
Conversion to open (%)
Bowel injuries: 2/51 (4) Urinary injuries: 1/51 (2) Vessel injuries: 2/51 (4) Urinary injuries: 1/21 (4.8) Vessel injuries: 2/21 (9.5) Post-op: Lymphocyst: 25/429 (6) l Post-op: Lymphocyst: 7/58 (12)$$ Intra-op: 0/97 Post-op: Lymphedema: 5/97 (5.2), Transient ascites: 3/97 (3.1), Chylous ascites: 3/97 (3.1), Small bowel obstruction: 1/97 (1), Hematoma 1/97 (1), Port site cellulites; 1/97 (1), Wound seroma: 1/97 (1) Intra-op: IMA injury: 2/32 (6.25) Post-op: Severe diarrhea: 1/32 (3.1), Ureteral leak: 1/32 (3.1) Post-op: Ileus: 2/30 (6.7), Port-site haematoma: 1/30 (3.3), Hemoperitoneum: 1/30 (3.3) Intra-op: Aortic injury: 1/22 (4.5) Post-op: Lymphocele: 2/22 (9), Port site hernia: 1/22 (4.5) Post-op: Lymphocele: 1/8 (12.5)
Complications (intra-op or post-op) (%)
–
Median (range): 3 (2–4)
Median (range): 6 (2–10)
NM
Y: 1/22
Median (IQR): 2 (2–3)
Median (IQR): 2 (2–5.2), p = 0.161
NM
Y: 1/32
NM
Mean (SD): 2.7 (0.8), p = 0.001
Mean (SD): 3.5 (1.9)
Mean (range): 5.6 (2–14), p = 0.049
Mean (range): 7.7 (2–40)
Hospital stay (in days)
N
NM
NM
NM
NM
NM
Follow up (in mo)
–
Y: 10/487
Y: 1/5, p = 0.26
Y: 9/18
Transfusion (Y/N)
NM
NM
NM
NM
NM
NM
NM
Recurrence
Arch Gynecol Obstet
NM
NM
Mean (range): 1 (0–4)
Zanagnolo [28]
Lambaudie [22]
Vizza [27]
NM
Mean (SD): 154.6 (171)
Mean (range): 50 (20–200)
Median (range): 67.5 (20–1800)
NM
5/19 (26)àà
7/52 (13.5)
NM
4/16 (25)àà
Kimmig [38]
Pakish [25]
EBL (in ml)
Nr of positive LNs
References
Table 2 continued
–
–
–
2/52 (3.9)
–
–
Conversion to open (%) Post-op: Vein thrombosis: 1/16 (6), Post-op aphasia 1/16 (6) Post-op: Lymphocele: 2/19 (11), Post-op bleeding: 1/19 (5), Port site infection: 1/19 (5) Intra-op: Vascular injury: 1/52 (1.9) Post-op: Respiratory infection: 1/52 (1.9), Urinary: 1/52 (1.9), Port site infection: 1/52 (1.9), Haematoma/lymphocele: 2/52 (3.9), Renal/urinary complications: 2/52 (3.9) Intra-op: Bleeding: 1/51 (3.9) Post-op: Chylous ascites: 7/51 (13.7), Vaginal leakage 2/51 (3.9), Ureteral fistula: 1/51 (1.9), Femoral nerve injury: 1/51 (1.9), Legs edema: 4/51 (7.8), Port-site hernia: 2/61 (3.9), Lymphocele: 4/51 (7.8), Lymphatic ascites 1/51 (1.9) Post-op: Lymphocele: 1/24 (4.2) Intra-op: Iliac vein injury: 1/20 (5) Post-op: Chylous ascites: 1/5 (20)
Complications (intra-op or post-op) (%)
Mean (range): 10.4 (1–21.6)
N
Median (range): 26 (1–56)
Y: 3/51 (5.8)
NM
NM
Y: 4/52 (7.7)
N
Median (range): 20 (12–28)
Median (range): 22 (13–28)
Follow up (in mo)
Y: 2/19
Y: 1/16
Transfusion (Y/N)
Median (range): 2 (1–4)
Mean (SD): 3.1 (1.6)
Median (range): 3 (2–7.5)
Mean: 2
Median (range): 9 (6–33)
Median (range): 10 (5–25)
Hospital stay (in days)
NM
NM
6/51 (11.7)
NM
1/19 (5)
2/16 (13)
Recurrence
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123
123
Mean (range): 2.6 (0–11)
Magrina [23]
2 5 2
–
–
1/8 (12.5)
NM
NM
NM
Recurrence
$$
$
##
#
Retroperitoneal group
Transperitoneal group
Cervical cancer patients and positive lymph nodes had adjuvant platinum-based chemotherapy/radiotherapy
Endometrial cancer patients (stage FIGO III) had six cycles of adjuvant platinum-based chemotherapy
Robotic-assisted transperitoneal (inframesenteric) group
Robotic-assisted transperitoneal (infrarenal) group
Conventional laparoscopic group
Refers to patients with positive lymph nodes
Calculated in weeks
Lymphadenectomy as isolated procedure In overall, regarding the total complications, no differences were found between the two groups (p = 0.31)
§§§
§§
§
àà
à
USA United States of America, y.o. years old, BMI body mass index, Nr number, EBL estimated blood loss, N No, Y yes, IMA inferior mesenteric artery, RTh radiotherapy, CTh chemotherapy, mo months, NM not mentioned, IQR interquartile range, DVT deep venous thrombosis, SCC squamous cell cervical carcinoma, SD standard deviation, NS not significant, MMMT malignant mixed Mu¨llerian tumour, UPSC uterine papillary serous carcinoma, LN lymph node
4
–
4
5
NM
1
N
Median (range): 1 (1–2)
2
Mean (range): 2.5 (1–13)
Hospital stay (in days)
7
NM
NM Mean (range): 12.8 (8–20)
N
NM
Follow up (in mo)
N
N
Transfusion (Y/ N)
–
–
Trocar site hernia: 1/5 (20)
Chylous ascites: 1/5 (20),
Post-op:
–
Lymphocele: 1/33 (3)
Post-op:
Bleeding: 1/33 (3)
Aorta injury: 1/33 (3),
Intra-op:
Complications (intra-op or post-op) (%)
–
NM
–
–
1/33 (3)
Conversion to open (%)
2
–
Fastrez [19]
Median (range): 150 (50–550)
200
Mean: 45
EBL (in ml)
–
1
NM
Chon [16]
Jacob [21]
Case reports
Nr of positive LNs
References
Table 2 continued
Arch Gynecol Obstet
Arch Gynecol Obstet
Techniques Extraperitoneal approach The inspection of peritoneal cavity is necessary in order to proceed to extraperitoneal lymphadenectomy. Through an umbilical transperitoneal port (10 mm trocar), the peritoneal cavity is inspected with the purpose to detect any intra-peritoneal lesions. A 15 mm incision is made at the left side of superior iliac spine. Through this incision and with blunt dissection of the abdominal muscles, the parietal fascia is accessed without opening the peritoneal fascia. The extraperitoneal space is created through digital dissection, which expands from the anterior surface of the lateral psoas muscle to the common iliac artery. A blunt-tip balloon trocar (10–12 mm) is placed through the incision for the introduction of the camera. Also, through this port, CO2 is insufflated with a stable pressure of 15 mmHg. An assistant port (10 mm) is positioned 1 cm above the corner of the pubic hair with the task to move ureters and ovarian vessels and to remove the endobag with the dissected lymph nodes. In addition, two additional trocars (8 mm) are placed both distal (8–10 cm) and medial (8–10 cm) to the camera port (one of which under the lowest rib on the anterior axillary line, at the level of umbilicus). The Da Vinci robotic system is situated contralateral to the side of the ports. Through the 8-mm ports, an ultrasonic harmonic scalpel and a bipolar forceps can be used. Lymph nodes located at para-aortic and preaortic regions are approached at zero degree. First and foremost, the identification of important structures (e.g. the aorta and its bifurcation, the vena cava, the ureters, the ovarian vessels) is fundamental before proceeding to the lymph node dissection. Before the removal of the trocars, a hole is created at the peritoneum anteriorly and laterally of the ureter to the intra-peritoneal cavity with the intention to avoid lymphocele. A drain is inserted above the pubis symphysis into the retroperitoneal space through the assistant port (10 mm). All the port entrances are closed with interrupted resorbable sutures, while the skin with nylon suture. Transperitoneal approach The Da Vinci robotic system is suggested to be placed at the head of the patient, while the patient is positioned in Trendelenburg position. The camera port (12 mm) is inserted 4 cm suprapubically and 2 cm laterally of the midline. Two additional trocars (10 mm) are placed 10–12 cm laterally to the camera port, and a third port is placed 12 cm laterally of the umbilicus. Monopolar scissors and a bipolar grasper are inserted via the two 10-mm ports. An accessory port can be placed between the camera
port and one of the additional 10-mm trocars, through which a fenestrated grasper could be inserted in order to retract the duodenum ventrally. After the entrance into the peritoneal cavity, the peritoneum over the midportion of the right common iliac artery is dissected up to the aortic bifurcation. A part of peritoneum is gently elevated ventrally with the use of grasping forceps, avoiding the entry of small bowel into the surgical field. Once having identified the aorta and its bifurcation, as well as the vena cava and the ureters, then the dissection of lymph nodes can be performed by removing initially the para-aortic and the interaortic nodes. The dissection is performed with excision of the lymph nodes over the vena cava. For the inframesenteric left aortic nodes, the peritoneal incision should be extended downwards from the aortic bifurcation to the left common iliac artery. At this point, in order to increase the exposure of both the inframesenteric left aortic nodes and the left infrarenal nodes, the inferior mesenteric artery may be transacted (before the transection of the artery, the viability of sigmoid should always be checked by temporarily clamping the inferior mesenteric artery). The dissection may be proceeded up to the left ovarian vein and the upper side of the left renal vein which can be considered, respectively, the lateral and upper limits of left aortic lymphadenectomy.
Discussion Assessment of the retroperitoneal lymph nodes is considered to be the standard of care in patients with gynaecological cancer. DaVinci robot can assist in the easier performance of such a technically challenging operation. The transperitoneal approach is the most widely used as the majority of the gynaecological oncologists are well trained to perform it; however, the extraperitoneal approach is increasingly used by well-trained teams worldwide. Till now, there is no comparison of the two methods and our review is trying to clarify the advantages and disadvantages of each technique. The extraperitoneal approach in comparison to the standard transperitoneal one presents a number of potential advantages. Firstly, the approach to the retroperitoneal space offers the possibility to limit and tamponate possible leaks of either blood or urine, avoiding the direct contact of urine or blood with bowel that can cause ileus [29]. The possibility of either vascular or intestinal injury is also decreased. Moreover, avoiding the entry into the peritoneal cavity can minimize the post-operative adhesions and hernia complications [30]. The CO2 insufflated into the working space is of lower pressure (about 12 mm Hg lower) and quantity in relation to the transperitoneal
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technique. Thus, complications related to CO2 passage into peritoneal cavity, such as subcutaneous emphysema, pneumothorax or even vagus nerve irritation, are quite negligible at the extraperitoneal technique. Moreover, the extraperitoneal approach reduces the necessity of extreme Trendelenburg position due to the fact that the abdominal viscera are retracted by peritoneum, offering a clear view of the surgical field. This is crucial in obese or elderly patients with comorbidities [31]. In particular, the decreased inclination during Trendelenburg position reduces the negative impact on ventilation and the usually increased peak pressure in the group of obese patients. However, the extraperitoneal technique may also present a few drawbacks. The restricted working space can be a serious issue especially for the not-so-experienced surgeons. In comparison to the transperitoneal approach, the port placement is one of the reasons that the operative time is usually prolonged, which can be easily interpreted into higher operating-room costs [25]. Moreover, the establishment of the retroperitoneal space and the detachment of peritoneum may create tension on various structures, such as the vesicourethral anastomosis [29]. In case of peritoneum tear during the formation of the working space and CO2 diffusion into the peritoneal cavity, an extra 5-mm port should be placed in the upper abdomen, in order to maintain steady the already-created surgical field. Utilizing the extraperitoneal approach, there is always the risk of creating lymphocele in case of pelvic lymphadenectomy, a probability that is insignificant after a transperitoneal approach where the lymphatic fluid can be absorbed and recycled within the peritoneal cavity [25, 31]. On the other hand, the transperitoneal approach may also present several advantages and disadvantages. The extensive working field and the relative easy port placement as well as the minimal risk of lymphocele are some of the strong points of the transperitoneal approach [31]. When bilateral lymphadenectomy is performed, the transperitoneal technique seems to be more efficient in comparison to the extraperitoneal approach which can be technically more challenging. Alternately, the potential disadvantages of the technique could include the risk of bowel injury or accidental perforation, the risk of vascular injuries, the probability of ileus due to a blood or urine leak and the need of severe Trendelenburg positioning of the patient which may have deep impact especially on patients with cardiopulmonary problems and increased intraocular pressure [16, 32]. As the role of extraperitoneal approach is already better clarified in urological patients, lessons could be learnt from their experience. For example, the presence of unilateral masses less than 5 cm diameter is an indication for minimally invasive extraperitoneal lymphadenectomy, and thus both laparoscopic- and robotic-assisted techniques have
123
oncological outcomes comparable to open surgery especially in the hands of experts [33]. Moreover, lymphocele may develop, in patients with prostatic carcinoma, when there is an invasion of the seminal vesicles or in cases of large tumour volume. Nevertheless, the scrupulous clipping of the lymphatic vessels does not always prevent the postoperative lymphocele [34, 35]. In an attempt to avoid this particular eventuality, some authors have proposed the formation of a peritoneal window after the completion of extraperitoneal lymphadenectomy in order to reduce the probability of lymphocele [36]. Various limitations should be taken into consideration in the evaluation of the findings of this paper. Some could argue that the main surgical approach in ovarian cancer is open surgery; however, there is a role of minimal invasive lymphadenectomies especially in fertility sparing procedures, and for this reason we included ovarian cancer in our analysis. The small number of the included studies, especially at the extraperitoneal approach in combination with the limited total number of the patients included, demonstrating that the evidence on the extraperitoneal lymphadenectomy is still new, and the improvement in the learning curve might differ the results. Besides that fact, trials with superior methodological quality (randomized control trials) are crucial in order to clarify technical details in both extraperitoneal and transperitoneal approaches. For example, we faced difficulties in performing such an analysis due to the heterogeneity of surgical approach in different institutions and the lack of a definition of what lymphadenectomy means leading to a range of retrieved nodes from 1 to 54 indicating a wide range of modifications of ‘‘lymphadenectomy’’. More specifically, it is very difficult to clarify from the included studies what each group means as pelvic or para-aortic lymph node dissection and where pelvic lymph node dissection ends or where paraaortic lymph node dissection starts. For this reason, we suggest that future randomized controlled trials should clarify with detailed definitions the inclusion criteria and the systematic approach of pelvic and para-aortic lymph node dissection in order to achieve better comparability of the surgery. Last but not least, even though our literature search presents wide range, it could be considered relatively selective by posing as limits the exclusion of abstracts, letters to the editor, surveys, reviews and animal studies. The restriction regarding the written language decreases further the number of the potentially included studies.
Conclusion In conclusion, robotic technology introduced a new dynamic in various surgical fields. The application of robotic-assisted surgery in complex operations of
Arch Gynecol Obstet
gynaecological oncology facilitated the pelvic and paraaortic lymphadenectomy. A reliable definition of the ‘‘kind’’ of lymphadenectomy used in each study is the first step in order to reach safe conclusions. Nevertheless, the lack of comparative studies, especially the randomized ones, cannot help us draw any safe conclusion regarding both the clinical outcomes and the possible superiority of extraperitoneal and transperitoneal approaches. Compliance with ethical standards Conflict of interest The authors declared no potential conflicts of interest with respect to the research, authorship and/or publication of this article.
References 1. Prasad SM, Shalhav AL (2013) Comparative effectiveness of minimally invasive versus open lymphadenectomy in urological cancers. Curr Opin Urol 23:57–64 2. Creasman WT, Morrow CP, Bundy BN, Homesley HD, Graham JE, Heller PB (1987) Surgical pathologic spread patterns of endometrial cancer. A Gynecologic Oncology Group Study. Cancer 60:2035–2041 3. Kilgore LC, Partridge EE, Alvarez RD et al (1995) Adenocarcinoma of the endometrium: survival comparisons of patients with and without pelvic node sampling. Gynecol Oncol 56:29–33 4. Mariani A, Webb MJ, Galli L, Podratz KC (2000) Potential therapeutic role of para-aortic lymphadenectomy in node-positive endometrial cancer. Gynecol Oncol 76:348–356 5. Delgado G, Bundy B, Zaino R, Sevin BU, Creasman WT, Major F (1990) Prospective surgical-pathological study of disease-free interval in patients with stage IB squamous cell carcinoma of the cervix: a Gynecologic Oncology Group study. Gynecol Oncol 38:352–357 6. Tanaka Y, Sawada S, Murata T (1984) Relationship between lymph node metastases and prognosis in patients irradiated postoperatively for carcinoma of the uterine cervix. Acta Radiol Oncol 23:455–459 7. Tinga DJ, Timmer PR, Bouma J, Aalders JG (1990) Prognostic significance of single versus multiple lymph node metastases in cervical carcinoma stage IB. Gynecol Oncol 39:175–180 8. Shah M, Lewin SN, Deutsch I et al (2011) Therapeutic role of lymphadenectomy for cervical cancer. Cancer 117:310–317 9. Burghardt E, Girardi F, Lahousen M, Tamussino K, Stettner H (1991) Patterns of pelvic and paraaortic lymph node involvement in ovarian cancer. Gynecol Oncol 40:103–106 10. Kigawa J, Minagawa Y, Itamochi H, Kanamori Y, Ishihara H, Terakawa N (1994) Retroperitoneal lymphadenectomy, including the para-aortic nodes in patients with stage III ovarian cancer. Am J Clin Oncol 17:230–233 11. Panici PB, Maggioni A, Hacker N et al (2005) Systematic aortic and pelvic lymphadenectomy versus resection of bulky nodes only in optimally debulked advanced ovarian cancer: a randomized clinical trial. J Natl Cancer Inst 97:560–566 12. Spirtos NM, Gross GM, Freddo JL, Ballon SC (1995) Cytoreductive surgery in advanced epithelial cancer of the ovary: the impact of aortic and pelvic lymphadenectomy. Gynecol Oncol 56:345–352 13. Iavazzo C, Darlas FM, Gkegkes ID (2013) The role of robotics in ovarian transposition. Acta Inform Med 21:135–137 14. Iavazzo C, Gkegkes ID (2014) Robotic technology for pelvic exenteration in cases of cervical cancer. Int J Gynaecol Obstet 125:15–17
15. Bats AS, Mimouni M, Bensaid C et al (2014) Robotic extraperitoneal paraaortic lymphadenectomy in gynecological cancers: feasibility, safety, and short-term outcomes of isolated and combined procedures. Int J Gynecol Cancer 24:1486–1492 16. Chon HS, Bush WD, Kang CW, Hoffman M (2013) Roboticassisted resection of isolated paraaortic lymph node recurrence with right lateral decubitus position. J Robotic Surg 7:205–207 17. Coronado PJ, Fasero M, Magrina JF, Herraiz MA, Vidart JA (2014) Comparison of perioperative outcomes and cost between robotic-assisted and conventional laparoscopy for transperitoneal infrarenal para-aortic lymphadenectomy (TIPAL). J Minim Invasive Gynecol 21:674–681 18. Fastrez M, Goffin F, Vergote I et al (2013) Multi-center experience of robot-assisted laparoscopic para-aortic lymphadenectomy for staging of locally advanced cervical carcinoma. Acta Obstet Gynecol Scand 92:895–901 19. Fastrez M, Vandromme J, George P, Rozenberg S, Degueldre M (2009) Robot assisted laparoscopic transperitoneal para-aortic lymphadenectomy in the management of advanced cervical carcinoma. Eur J Obstet Gynecol Reprod Biol 147:226–229 20. Gorostidi M, Larreategui J, Bernal T et al (2014) Robotic retroperitoneal paraaortic lymphadenectomy at Donostia University Hospital. J Minim Invasive Gynecol 21:480–485 21. Jacob KA, Zanagnolo V, Magrina JF, Magtibay PM (2011) Robotic transperitoneal infrarenal aortic lymphadenectomy for gynecologic malignancy: a left lateral approach. J Laparoendosc Adv Surg Tech A 21:733–736 22. Lambaudie E, Narducci F, Leblanc E et al (2012) Robotically assisted laparoscopy for paraaortic lymphadenectomy: technical description and results of an initial experience. Surg Endosc 26:2430–2435 23. Magrina JF, Long JB, Kho RM, Giles DL, Montero RP, Magtibay PM (2010) Robotic transperitoneal infrarenal aortic lymphadenectomy: technique and results. Int J Gynecol Cancer 20:184–187 24. Narducci F, Lambaudie E, Houvenaeghel G, Collinet P, Leblanc E (2009) Early experience of robotic-assisted laparoscopy for extraperitoneal para-aortic lymphadenectomy up to the left renal vein. Gynecol Oncol 115:172–174 25. Pakish J, Soliman PT, Frumovitz M et al (2014) A comparison of extraperitoneal versus transperitoneal laparoscopic or robotic para-aortic lymphadenectomy for staging of endometrial carcinoma. Gynecol Oncol 132:366–371 26. Vergote I, Pouseele B, Van Gorp T et al (2008) Robotic retroperitoneal lower para-aortic lymphadenectomy in cervical carcinoma: first report on the technique used in 5 patients. Acta Obstet Gynecol Scand 87:783–787 27. Vizza E, Mancini E, Baiocco E et al (2012) Robotic transperitoneal aortic lymphadenectomy in gynecologic cancer: a new robotic surgical technique and review of the literature. Ann Surg Oncol 19:3832–3838 28. Zanagnolo V, Rollo D, Tomaselli T et al (2013) Robotic-assisted transperitoneal aortic lymphadenectomy as part of staging procedure for gynaecological malignancies: single institution experience. Obstet Gynecol Int 2013:931318 29. Madi R, Daignault S, Wood DP (2007) Extraperitoneal v intraperitoneal robotic prostatectomy: analysis of operative outcomes. J Endourol 21:1553–1557 30. Huang M, Slomovitz BM, Ramirez PT (2009) Transperitoneal versus extraperitoneal para-aortic lymphadenectomy in patients with cervical cancer. Rev Obstet Gynecol 2:101–106 31. Atug F, Castle EP, Woods M, Srivastav SK, Thomas R, Davis R (2006) Transperitoneal versus extraperitoneal robotic-assisted radical prostatectomy: is one better than the other? Urology 68:1077–1081
123
Arch Gynecol Obstet 32. Gkegkes ID, Karydis A, Tyritzis SI, Iavazzo C (2014) Ocular complications in robotic surgery. Int J Med Robot 33. Kunit T, Janetschek G (2014) Laparoscopic and robotic postchemotherapy retroperitoneal lymph node dissection. Curr Opin Urol 24:162–167 34. Ghazi A, Scosyrev E, Patel H, Messing EM, Joseph JV (2013) Complications associated with extraperitoneal robot-assisted radical prostatectomy using the standardized Martin classification. Urology 81:324–331 35. Lee JY, Diaz RR, Cho KS et al (2013) Lymphocele after extraperitoneal robot-assisted radical prostatectomy: a propensity score-matching study. Int J Urol 20:1169–1176 36. Stolzenburg JU, Wasserscheid J, Rabenalt R et al (2008) Reduction in incidence of lymphocele following extraperitoneal radical prostatectomy and pelvic lymph node dissection by bilateral peritoneal fenestration. World J Urol 26:581–586 37. Wimberger P, Lehmann N, Kimmig R, Burges A, Meier W, Du Bois A (2007) Arbeitsgemeinschaft Gynaekologische Onkologie Ovarian Cancer Study Group. Prognostic factors for complete debulking in advanced ovarian cancer and its impact on survival. An exploratory analysis of a prospectively randomized phase III study of the Arbeitsgemeinschaft Gynaekologische Onkologie
123
38.
39.
40.
41.
Ovarian Cancer Study Group (AGO-OVAR). Gynecol Oncol 106:69–74 Kimmig R, Iannaccone A, Buderath P, Aktas B, Wimberger P, Heubner M (2013) Definition of compartment based radical surgery in uterine cancer-part I: therapeutic pelvic and periaortic lymphadenectomy by Michael ho¨ckel translated to robotic surgery. ISRN Obstet Gynecol 25:1–17 James JA, Rakowski JA, Jeppson CN, Stavitzski NM, Ahmad S, Holloway RW (2015) Robotic transperitoneal infra-renal aortic lymphadenectomy in early-stage endometrial cancer. Gynecol Oncol 136:285–292 Hudry D, Ahmad S, Zanagnolo V, Narducci F, Fastrez M, Ponce J, Tucher E, Le´curu F, Conri V, Leguevaque P, Goffin F, Holloway RW (2015) Lambaudie E; SERGS Group. Robotically assisted para-aortic lymphadenectomy: surgical results: a cohort study of 487 patients. Int J Gynecol Cancer 25:504–511 Akladios C, Ronzino V, Schrot-Sanyan S, Afors K, Fernandes R, Baldauf JJ, Wattiez A (2015) Comparison between transperitoneal and extraperitoneal laparoscopic paraaortic lymphadenectomy in gynecologic malignancies. J Minim Invasive Gynecol 22:268–274
