Introduction
Advances in diagnostic imaging modalities have increased the detection of more than one primary tumour in the same patient. The second tumour may be asymptomatic or incidental. For epidemiological studies, tumours are considered multiple primary malignancies if they are found in different sizes and are of a different histology or morphology group, excluding metastatic lesions (1). Interestingly, urological cancers presenting as the second primary have been reported to be in the range of 3.3–6.6% (2). Synchronous tumours refer to cases in which the second primary cancer is diagnosed within 6 months of primary cancer.
When surgery is the primary treatment, excision of both tumours using conventional open surgery in one sitting is challenging. Hence, most surgeons look at minimal invasive, either laparoscopic or robotic, techniques to complete surgical treatment (3). Boni et al. reported several advantages of robotic surgery in the management of multiple primary tumours involving the genitourinary tract (4). These patients experienced a shorter hospitalisation, early postoperative recovery, and better cosmetic results. Despite these advantages, extraction of the specimen needs a small incision with some chance of incisional hernia and scar. Natural orifice specimen extraction (NOSE) through the transvaginal or transanal route has been described to reduce the morbidity of hernia and scar. Breda et al. in 1993 were the first to report transvaginal extraction of intact kidneys after laparoscopic nephrectomy (5). Gill et al. in 2002 demonstrated the safety and feasibility of NOSE in ten cases of renal cancer after laparoscopy (6). Recent case series have successfully shown NOSE in colorectal neoplasms using a robotic platform (7–9).
We have previously published a case report of natural orifice specimen extraction of synchronous tumours involving the genitourinary and gynaecological tract using a robotic platform (10). The present article aims to report our updated experience of managing five patients with two synchronous tumours/lesions involving two quadrants with the help of a robotic platform (da Vinci SHD) and extraction of both specimens using the NOSE technique.
Materials and Methods
We undertook a retrospective study of five female patients with synchronous (renal and uterine) tumours presenting to a single institute from 2015 to 2018. Three patients had synchronous renal cell carcinoma with endometrial carcinoma, and two patients had synchronous renal cell carcinoma with fibroid uterus with dysfunctional uterine bleed. The study was conducted after institutional ethics clearance.
All cases had operable primary tumours, and the decision for surgery was taken after institutional board review. Furthermore, we included patients opting for the removal of both the tumours in a single sitting. A single experienced onco-surgeon (author no. 2) operated on all cases using the da Vinci SHD-robot. The details of the technique are given below.
Technique
As per protocol, the surgery sequence was to excise the renal tumour first and the uterine next. Initially, the patient was positioned in a plank position with the table moderately flexed. Pneumoperitoneum was established using a Veress needle, either in the periumbilical region/Palmer’s point on the left side and McBurney’s point on the right side. Four/five ports were placed: a 12-mm periumbilical camera port, an 8-mm subcostal robotic trocar in the midclavicular line, an 8-mm robotic trocar in the midaxillary line above the iliac crest, and one 12-mm assistant trocar in the low midline to allow passage of sutures, stapler devices, suction, or retraction (Fig. 1). We used an additional 5 mm sub-xiphoid trocar, if necessary, for robot-assisted right radical nephrectomy. Using a three-arm configuration, the robot was docked, and the nephrectomy was performed. After bagging the nephrectomy specimen, the robot was undocked. Later, maintaining the ports in a sterile setup, the patient was placed in lithotomy position, and an additional 8 mm lumbar port was inserted (Fig. 2). The robot was docked between the legs. Total hysterectomy with or without adnexa was done without a manipulator. Bilateral pelvic node dissection was done in three patients with endometrial cancer. Adequate colpotomy was done to deliver the uterus first and renal mass with the bag next, per vaginum. In two patients, colpotomy had to be widened posteriorly to accommodate a sizeable renal mass (Fig. 3). The colpotomy was closed with continuous V-Loc sutures. Port site defects were closed with nylon sutures (Fig. 4). In a video published by the author, details of port placements and the procedure in patient number 5 have been described (9).
Fig. 1.

Port positions in left lateral position for robot-assisted radical nephrectomy
Fig. 2.

Port position in modified left lateral position for robot-assisted radical hysterectomy
Fig. 3.

Specimen of patient no. 5
Fig. 4.

Postoperative day 8 appearance in patient no. 5
We studied the demographic data, presenting symptoms, staging, and procedure performed for each patient. At the time of surgery, we noted short-term outcomes, including operative time and blood loss. We calculated the mean hospital stay, mean time to ambulation, and mean pain score on postoperative day 5 after surgery. A numerical rating pain analog scale was used, calculated from 0 to 10: 0: no pain; 1–3: mild pain; 4–6: moderate pain; 7–10: severe pain. A mean pain score was calculated in each patient depending on the duration of admission.
Postoperatively, the histopathology report, adjuvant treatment, and follow-up protocol were noted.
Results
A total of five patients were operated on for synchronous renal and uterine tumours. The mean age in these patients was 56 years—all patients presented with dysfunctional uterine bleed. Two out of the three patients presented with vague flank pain, but none had hematuria. All patients were multiparous and perimenopausal.
The staging of renal cancer was based on the tumour-node-metastasis (TNM) staging system, and endometrial cancer was based on the International Federation of Gynecology and Obstetrics tumor-node-metastasis staging system. Staging renal cancer was done using triple-phase CT and staging of endometrial cancer was done using hysteroscopy with endometrial sampling and MRI pelvis.
The staging and procedure performed are summarised in Table 1.
Table 1.
Staging and procedure of the renal and uterine tumours based on TNM and FIGO staging, respectively
| Patient 1 | Patient 2 | Patient 3 | Patient 4 | Patient 5 | |
|---|---|---|---|---|---|
| Renal | cT2bN0M0 | cT2aN0M0 | cT2bN0M0 | cT2bN0M0 | cT2bN0M0 |
| Uterine | Stage Ia | Stage Ia | Fibroid | Stage Ib | Fibroid |
| Procedure (robot assisted) | Right radical nephrectomy + Radical hysterectomy + BPLND | Left partial nephrectomy + Radical hysterectomy + BPLND | Left radical nephrectomy + Total hysterectomy | Right radical nephrectomy + Radical hysterectomy + BPLND | Left radical nephrectomy + Total hysterectomy |
Perioperative descriptive analysis of the procedures performed is shown in Table 2.
Table 2.
Perioperative descriptive analysis of the procedures performed
| Mean operative time (minutes) | 111.6 (± 25.4 SD) |
|---|---|
| Mean blood loss (ml) | 70.2 (± 6.6 SD) |
| Mean pain score on POD5 | 3.8 ± 1.2 |
| Meantime to ambulation (days) | 2.7 (± 0.8 SD) |
| Mean hospital stay (days) | 5.6 (± 1.9 SD) |
The postoperative complications were limited to Clavien-Dindo grade I complications.
Histopathology results and additional remarks are given in Table 3.
Table 3.
Histopathology results of the specimen in each patient
| The mean number of pelvic lymph nodes removed | 17.0 ± 8.3SD | ||||
|---|---|---|---|---|---|
| Patient 1 | Patient 2 | Patient 3 | Patient 4 | Patient 5 | |
| Renal specimen (gross findings/pathological TNM staging) | pT2aNxM0 | pT2aNxM0 | pT2b0NxM0 | pT2bNxM0 | pT3aNxM0 (renal vein thrombus) |
| Renal specimen (microscopic findings) | Clear cell carcinoma, Fuhrman grade 2 | Clear cell carcinoma, Fuhrman grade 1 | Clear cell carcinoma, Fuhrman grade 3 | Papillary cell carcinoma, Fuhrman grade 3 | Chromophobe carcinoma |
| Endometrium (gross findings/FIGO staging) | IB | IB | Thickened endometrium with the presence of submucosal leiomyoma | IB | Thickened endometrium with the presence of submucosal leiomyoma |
| Endometrium (histologic grade, endometrioid histology) | G2 | G2 | Atypical endometrial hyperplasia with uterine leiomyoma | G3 | Atypical endometrial hyperplasia with uterine leiomyoma |
| Additional remarks | Received adjuvant EBRT | Received adjuvant EBRT | Nil | Received adjuvant EBRT | Nil |
Post-surgery, patients were followed up using clinical assessment, blood biochemistry, chest X-ray, and CT of the abdomen and pelvis at 3 and 6 months, then every 6 months for 3 years then yearly. None of the patients had incisional site hernia nor port site relapse. All patients were recurrence-free at 36–60 months post-surgery. Three patients had dyspareunia and the reason postulated is the generous colpotomy and adjuvant radiotherapy or both, which may have led to vaginal shortening and scarring.
Discussion
With the increase in the number of patients presenting with synchronous tumours, surgical management is becoming more complex. These tumours may be in different locations or quadrants, adding to the further technical glitches. Traditionally, these patients were offered open surgery in two sittings. Furthermore, if one of the tumours needs immediate adjuvant therapy, the second surgery may have to be deferred. Post adjuvant treatment, the second surgery may be challenging.
With the advent of minimal invasive surgery in the early 1980s, surgeons have been exploring the possibility of combining two surgeries in one sitting (11). Also, many patients prefer both surgeries in one sitting for various logistical and economic reasons. Currently, MIS has passed the rider of oncological safety, feasibility, and reduced morbidity; hence, it is logical to consider this approach in managing two synchronous tumours. Several authors have reported the successful use of the laparoscopic platform in managing them. Recently, others have gone further and showed the use of the robotic platform with similar benefits in colorectal surgeries (4, 9, 12–16). In technically challenging cases such as these, surgeons performing robotic and laparoscopic surgeries agree that robotic surgery has advantages with better stereoscopic vision, superior instruments with seven degrees of freedom, and motion scaling compared to laparoscopic instruments which improves surgical dissection and prevents conversion to open (17). The short learning curve compared to laparoscopy, ease of doing complex cases that would have otherwise required open surgery, and increased demand from patients also contribute to the increase in robotic procedures. Despite the higher costs, the advantage of robotic surgery can be seen when reimbursement shifts from a “fee for service” model to a “value-based” model that values quality of care and better outcomes (18). The da Vinci Xi model is particularly advantageous in performing multi-quadrant surgeries. The rotating boom can be set to any position relative to the patient and targeted to a particular anatomy. Longer, thinner, and parallel working arms facilitate less restrictive trocar placement in multi-quadrant procedures, making hybrid procedures obsolete (19).
As minimally invasive surgery became widespread, specimen extraction required an additional incision, albeit small, with potential for incisional hernia at the site. Gill et al. described transvaginal extraction of ten laparoscopic radical nephrectomy specimens in 2002 (6). The specimen was extracted intact via the vagina, and the posterior colpotomy incision was repaired transvaginally. The authors postulated that specimens weighing up to 500 g and 7 cm across can be removed via a 3–4 cm incision on the vaginal dome due to inherent pliability of the vaginal tissue. The benefits of NOSE in colorectal malignancies have been widely studied. Nishimura et al. described that all patients who experienced NOSE in their study could walk on a postoperative day 1 (20). In the study by Park et al., advantages of transvaginal extraction included less pain, less intra-operative blood loss, faster recovery of intestinal function, lower complication rate, and cosmetic effect (21). These studies involved removal of intact specimen through a colpotomy without concomitant hysterectomy. Posterior vaginal colpotomy is easier but gives a tight colpotomy due to uterosacral attachments and occasional bleeding from the deep uterine vein. Transvaginal extraction requires technical expertise, extended operation time, and is obviously limited to female patients which is the major hindrance in its widespread use (22). Lastly, there are only few reports of sexual dysfunction after specimen extraction through the vagina so far. Palanivelu et al. found no dyspareunia in any of the eleven patients in their series after 1 year of follow-up (23). Kim et al. demonstrated no rectovaginal fistulas or dyspareunia at 3-month follow-up in 58 patients who underwent transvaginal specimen extraction (24).
Yao et al. described, for the first time, NOSE using the robotic platform without additional specialised instrumentation for colorectal neoplasms (8). They compared the previous reports on laparoscopic NOSE with their study and revealed the advantages of robotic NOSE in safety and feasibility. One can surmise from the above literature that NOSE is a viable option for extracting at least one specimen. All these studies reported single tumour/specimen extraction. Hillyer et al. demonstrated that a robotic platform is a safe and effective minimally invasive nephron-sparing treatment of bilateral synchronous kidney tumours (15).
Our study highlights the beneficial use of a robotic platform in treating synchronous renal and endometrial tumours in a selected group of females with several advantages, as described earlier. Secondly, we believe in the utility of NOSE as a further step in extracting more than one specimen with moderate size without performing a mini laparotomy. A posterior colpotomy may be needed depending on the size of the specimen. Thirdly, we advocate that RARN (nephrectomy) be performed first to overcome the physiological and hemodynamic challenges after a nephrectomy. One additional 8 mm port in the opposite flank is enough once the patient changes to a supine position regarding the port placement. RARH, as the second procedure, maintains pneumoperitoneum throughout the procedure and allows aborting the operation, if required, after completing the critical half first.
Thus, we feel that the robotic platform due to its benefits is the most ideal for this clinical situation. Furthermore, with this approach, adjuvant therapy can be started in the early postoperative period. Simultaneous surgery has better cost-effectiveness, and reduced psychological and surgery-related stress.
Our study shows superior outcomes in postoperative pain control, time to first bowel function, hospital stay, reduced incisional hernia, and better cosmesis in robot-assisted surgery with NOSE. Oncological outcomes are comparable with no relapses in our series. We want to caution that patient selection plays a significant role in taking advantage of this evolution in minimally invasive surgery. The benefits of NOSE in robotic surgery of synchronous tumours need further study, mainly to determine if the reported benefits can be applied to other synchronous tumours.
Conclusion
Robotic natural orifice specimen extraction (NOSE) has distinct advantages, including less blood loss, less pain, and a shorter hospital stay than open surgery and minimal scar of SE, at least in females. Our experience demonstrates the feasibility of two-quadrant robotic surgery involving two different organs in the same sitting without compromising the oncological outcome. Future comparative studies, including larger patient cohorts and longer follow-up, will define the ultimate role of this novel approach to the robotic platform.
Abbreviations
- NOSE
Natural orifice specimen extraction
- TNM
Tumour node metastasis
- G
Grade
- CT
Computed tomography
- MRI
Magnetic resonance imaging
- BPLND
Bilateral pelvic lymph node dissection
- SD
Standard deviation
- POD
Postoperative day
- EBRT
External beam radiotherapy
- SE
Specimen extraction
- RARN
Robot-assisted radical nephrectomy
- RARH
Robot-assisted radical hysterectomy
Declarations
Conflict of Interest
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Contributor Information
Neeraja Tillu, Email: drneerjatillu@gmail.com.
Jagdeesh Kulkarni, Email: drjnkulkarni@gmail.com.
References
- 1.Vogt A, Schmid S, Heinimann K, Frick H, Herrmann C, Cerny T, et al. Multiple primary tumours: challenges and approaches, a review. ESMO Open. 2017;2(2):e000172. doi: 10.1136/esmoopen-2017-000172. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Donin N, Filson C, Drakaki A, Tan HJ, Castillo A, Kwan L, et al. Risk of second primary malignancies among cancer survivors in the United States, 1992 through 2008. Cancer. 2016;122(19):3075–3086. doi: 10.1002/cncr.30164. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Jørgensen SL, Mogensen O, Wu C, Lund K, Iachina M, Korsholm M, et al. Nationwide introduction of minimally invasive robotic surgery for early-stage endometrial cancer and its association with severe complications. JAMA Surg. 2019;154(6):530. doi: 10.1001/jamasurg.2018.5840. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Boni A, Cochetti G, Ascani S et al (2018) Robotic treatment of oligometastatic kidney tumor with synchronous pancreatic metastasis: case report and review of the literature. BMC Surg 18(1):40. 10.1186/s12893-018-0371-x [DOI] [PMC free article] [PubMed]
- 5.Breda G, Silvestre P, Giunta A, Xausa D, Tamai A, Gherardi L (1993) Laparoscopic nephrectomy with vaginal delivery of the intact kidney. Eur Urol 24(1):116–7. 10.1159/000474276 [DOI] [PubMed]
- 6.Gill IS, Cherullo EE, Meraney AM, Borsuk F, Murphy DP, Falcone T (2002) Vaginal extraction of the intact specimen following laparoscopic radical nephrectomy. J Urol 167(1):238–41 [PubMed]
- 7.Park JS, Choi GS, Kim HJ, Park SY, Jun SH (2011) Natural orifice specimen extraction versus conventional laparoscopically assisted right hemicolectomy. Br J Surg 98(5):710–5. 10.1002/bjs.7419 [DOI] [PubMed]
- 8.Yao H, Li T, Chen W, Lei S, Liu K, Liu B, Zhou J (2021) Role of robotic natural orifice specimen extraction surgery in colorectal neoplasms. Sci Rep 11(1):9818. 10.1038/s41598-021-89323-z [DOI] [PMC free article] [PubMed]
- 9.Feng Q, Ng SSM, Zhang Z, Lin S, Niu Z, Wei Y, He G, Chang W, Zhu D, Xu J (2021) Comparison between robotic natural orifice specimen extraction surgery and traditional laparoscopic low anterior resection for middle and low rectal cancer: A propensity score matching analysis. J Surg Oncol 124(4):607–618. 10.1002/jso.26552 [DOI] [PubMed]
- 10.Kulkarni JN, Maurya N, Bhukte S, Karanjgaokar V. Robot assisted radical nephrectomy + hysterectomy and specimen retrieval per vaginum (nOSE) Int Braz J Urol. 2019;45(3):45–45. doi: 10.1590/S1677-5538.IBJU.2018.0351. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Siddaiah-Subramanya M, Tiang KW, Nyandowe M (2017) A New Era of Minimally Invasive Surgery: Progress and Development of Major Technical Innovations in General Surgery Over the Last Decade. Surg J (N Y) 3(4):e163–e166. 10.1055/s-0037-1608651 [DOI] [PMC free article] [PubMed]
- 12.Dwyer RH, Scheidt MJ, Marshall JS, Tsoraides SS (2018) Safety and efficacy of synchronous robotic surgery for colorectal cancer with liver metastases. J Robot Surg 12(4):603–606. 10.1007/s11701-018-0813-6 [DOI] [PubMed]
- 13.Suh BJ, Oh SJ, Shin JY et al (2017) Simultaneous robotic subtotal gastrectomy and right hemicolectomy for synchronous adenocarcinoma of stomach and colon. J Robotic Surg 11(3):377–380. 10.1007/s11701-017-0681-5 [DOI] [PMC free article] [PubMed]
- 14.Imagami T, Takayama S, Hattori T, Matsui R, Sakamoto M, Kani H, Kurokawa S, Fujiwara T (2018) Combined laparoscopic and robotic surgery for synchronous colorectal and genitourinary cancer: A case series. Int J Surg Case Rep 51:323–327. 10.1016/j.ijscr.2018.09.021 [DOI] [PMC free article] [PubMed]
- 15.Hillyer SP, Autorino R, Laydner H, Yang B, Altunrende F, White M, Spana G, Khanna R, Isac W, Hernandez AV, Simmons M, Stein R, Haber GP, Kaouk J (2011) Robotic versus laparoscopic partial nephrectomy for bilateral synchronous kidney tumors: single-institution comparative analysis. Urology 78(4):808–12. 10.1016/j.urology.2011.06.012 [DOI] [PubMed]
- 16.Ong KH, Huang SK, Yen CS, Tian YF, Sun DP (2016) Simultaneous Retroperitoneal Robotic Partial Nephrectomy and Hepatectomy for Synchronous Renal-Cell Carcinoma and Hepatocellular Carcinoma in a Cirrhotic Patient. J Endourol Case Rep 2(1):215–217. 10.1089/cren.2016.0096 [DOI] [PMC free article] [PubMed]
- 17.Toh JWT, Phan K, Kim SH. Robotic colorectal surgery: more than a fantastic toy? Innov Surg Sci. 2018;3(1):65–68. doi: 10.1515/iss-2017-0046. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Perez RE, Schwaitzberg SD. Robotic surgery: finding value in 2019 and beyond. Ann Laparosc Endosc Surg. 2019;4:51–51. doi: 10.21037/ales.2019.05.02. [DOI] [Google Scholar]
- 19.Scotton G, Contardo T, Zerbinati A, Tosato SM, Orsini C, Morpurgo E. From laparoscopic right colectomy with extracorporeal anastomosis to robot-assisted intracorporeal anastomosis to totally robotic right colectomy for cancer: the evolution of robotic multiquadrant abdominal surgery. J Laparoendosc Adv Surg Tech. 2018;28(10):1216–1222. doi: 10.1089/lap.2017.0693. [DOI] [PubMed] [Google Scholar]
- 20.Nishimura A, Kawahara M, Suda K, Makino S, Kawachi Y, Nikkuni K (2011) Totally laparoscopic sigmoid colectomy with transanal specimen extraction. Surg Endosc 25(10):3459–63. 10.1007/s00464-011-1716-z [DOI] [PubMed]
- 21.Park JS, Kang H, Park SY, Kim HJ, Lee IT, Choi GS (2018) Long-term outcomes after Natural Orifice Specimen Extraction versus conventional laparoscopy-assisted surgery for rectal cancer: a matched case-control study. Ann Surg Treat Res 94(1):26–35. 10.4174/astr.2018.94.1.26 [DOI] [PMC free article] [PubMed]
- 22.Han FH. Transanal natural orifice specimen extraction for laparoscopic anterior resection in rectal cancer. World J Gastroenterol. 2013;19(43):7751. doi: 10.3748/wjg.v19.i43.7751. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Palanivelu C, Rangarajan M, Jategaonkar PA, Anand NV (2008) An innovative technique for colorectal specimen retrieval: a new era of "natural orifice specimen extraction" (N.O.S.E). Dis Colon Rectum 51(7):1120–4. 10.1007/s10350-008-9316-2 [DOI] [PubMed]
- 24.Kim HJ, Choi GS, Park JS, Park SY, Ryuk JP, Yoon SH (2014) Transvaginal specimen extraction versus conventional minilaparotomy after laparoscopic anterior resection for colorectal cancer: mid-term results of a casematched study. Surg Endosc 28(8):2342–8. 10.1007/s00464-014-3466-1 [DOI] [PubMed]
