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Übersicht

Robotic Liver Surgery – Current Standards and Future Perspectives


Robotische Leberchirurgie – Aktuelle Standards und Perspektiven

Authors
Felix Becker, Haluk Morgül, Shadi Katou, Mazen Juratli, Jens Peter Hölzen, Andreas Pascher, Benjamin Struecker

Affiliation laparoskopischen sowie robotischen Leberchirurgie bietet


Department of General, Visceral and Transplant Surgery, diese Übersichtsarbeit einen Überblick über aktuelle Literatur
University Hospital Münster, Germany sowie Standards und zielt darauf ab, zukünftige Entwicklun-
gen der robotischen Leberchirurgie aufzuzeigen.
Key words
Ergebnisse Die robotische Leberchirurgie ist ein sicheres und
liver, hepatic resection, robotic surgery, minimal invasive
technisch durchführbares Operationsverfahren. Im Vergleich
surgery, laparoscopy
zu offener und laparoskopischer Chirurgie zeigen sich verbes-
Schlüsselwörter serte intra- und postoperative Outcome Daten, bei gleichwer-
Leber, Leberresektion, robotische Chirurgie, Minimal invasive tigen onkologischen Ergebnissen.
Chirurgie Diskussion In komplexen Fällen, einschließlich größerer

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Hepatektomien, erweiterter Gallenrekonstruktionen und Seg-
received 31.10.2020 mentektomien der hinteren Segmente, stellt sich robotische
accepted 03.12.2020 Chirurgie mehr als Alternative zur offenen als zur laparoskopi-
schen Chirurgie auf. Damit erweitert sich das Spektrum mini-
Bibliography
malinvasiver Leberchirurgie.
Z Gastroenterol 2021; 59: 56–62
DOI 10.1055/a-1329-3067 ABSTR AC T
ISSN 0044-2771
Background Robotic liver surgery is emerging as the future
© 2020. Thieme. All rights reserved.
of minimal invasive surgery. The robotic surgical system offers
Georg Thieme Verlag KG, Rüdigerstraße 14,
a stable camera platform, elimination of physiologic tremor,
70469 Stuttgart, Germany
augmented surgical dexterity as well as improved ergonomics
Correspondence because of a seated operating position. Due to the theoretical
Felix Becker advantages of the robotic assisted system, complex liver sur-
Department of General, Visceral and Transplant Surgery gery might be an especially interesting indication for a robotic
University Hospital Münster, Waldeyerstraße 1, approach since it demands delicate tissue dissection, precise
48149 Münster, Germany intracorporeal suturing as well as difficult parenchymal tran-
Tel.: +49/2 51/8 35 63 01 section with subsequent need for meticulous hemostasis and
Fax: +49/2 51/8 35 63 11 biliostasis.
felix.becker@ukmuenster.de Material and methods An analysis of English and German
literature on open, laparoscopic and robotic liver surgery was
Z US A M M E N FA SS U N G performed and this review provides a general overview of the
Hintergrund Die robotische Leberchirurgie entwickelt sich existing literature along with current standards and aims to
zur Zukunft der minimalinvasiven Chirurgie. Das robotische specifically point out future directions of robotic liver surgery.
Operationssystem bietet eine stabile Kameraplattform, Elimi- Results Robotic liver surgery is safe and feasible compared to
nation des physiologischen Tremors, verbesserte chirurgische open and laparoscopic surgery, with improved short-term
Geschicklichkeit sowie eine entspannte Ergonomie durch postoperative outcomes and at least non-inferior oncological
sitzende Position. Aufgrund theoretischer Vorteile des robot- outcomes.
ergestützten Systems erscheint die Leberchirurgie ein beson- Conclusion In complex cases including major hepatectom-
ders geeignetes Feld für den Einsatz des OP Roboters zu sein, ies, extended hepatectomies with biliary reconstruction and
da es hohe technische Anforderung (delikate vaskuläre und difficult segmentectomies of the posterior-superior seg-
parenchymatöse Präparation, intrakoroprale Anastomosen, ments, robotic surgery appears to emerge as a reasonable
Blutstillung) an den Chirurgen stellt. alternative to open surgery rather than being an alternative
Material und Methoden Durch die Auswertung bestehen- to laparoscopic procedures.
der englisch- und deutschsprachigen Literatur zur offenen,

56 Becker F et al. Robotic Liver Surgery… Z Gastroenterol 2021; 59: 56–62 | © 2020. Thieme. All rights reserved.
Introduction Current standards
Over the last decades, minimal invasive hepatic resection has The standard approach in modern liver surgery should be a mini-
revolutionized the landscape of liver surgery. Various inherent mal invasive one, complemented by hybrid and hand-assisted
drawbacks of conventional surgery were attenuated, and mini- strategies or open resections for highly complex cases. Benefits
mally invasive approaches in liver surgery have been shown to of- of minimal invasive over conventional open liver surgery have
fer specific advantages including reduced blood loss, fewer inci- been well established [12, 13], including reduced intraoperative
sional hernias, minimized morbidity and postoperative pain, blood loss, reduced postoperative pain, shorter length of stay
decreased time to postoperative oral intake, shorter length of and lower risk for perioperative complications in combination
stay and improved cosmesis as well as enhanced cost-effective- with a non-inferiority in oncological results. These advantages
ness. [1]. In addition, a growing body of evidence reveals that are currently reflected by recommendations from the 2018
laparoscopic surgery can be superior to conventional open sur- Southampton consensus guidelines for laparoscopic liver surgery,
gery without compromising oncologic outcomes (R0 resection stating a clear indication for minimal invasive approaches for cer-
rate and 5-year overall survival), even for complex malignant dis- tain resections (left lateral and anterior segments) [14]. This is
eases such as colorectal liver metastasis or hepatocellular carcino- in accordance with the 2008 Louisville [15] and updated 2014
ma [2–4]. However, although minimal invasive surgery should be Morioka statement [16].
the standard approach for the majority of hepatic resections,
many centers still perform open liver surgery. This can partly Is Robotic Surgery an Extension to Laparoscopy
be explained with intrinsic limitations of the laparoscopic ap- or Alternative to Open Resection?
proach [5]: 1) an unsteady and only two-dimensional view, 2) am- The pattern of establishing robotic liver surgery followed the trend
plification of physiologic tremor, 3) limited mobility due to

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of laparoscopic liver surgery, starting with benign (e. g. focal nodu-
straight instruments in combination with a limited range of lar hyperplasia, hemangioma, or hepatocellular adenoma) or
motion, 4) poor ergonomics for the surgical team and 5) longer peripherally located lesions (left lateral section (II, III) or anterior he-
operation times. Robotic surgery could overcome many of these patic segments (IVb, V, VI)) with progression to more advanced
limitations and provides the unique chance to complement procedures including major hepatectomies and resections of pos-
laparoscopic approaches in liver surgery; moreover, robotic liver tero-superior segments (IVa, VII, VIII). Although safety and feasibil-
surgery will challenge open liver resections for indications, cur- ity of laparoscopic resections of the postero-superior segments as
rently doomed as not feasible for a minimal invasive procedure. well as major resections have been thoroughly established by spe-
The robotic surgical system offers a stable, high-definition and cialist centers over the last decade, these procedures are still
magnified three-dimensional camera platform, elimination of conducted mainly as open resections in most peripheral centers.
physiologic tremor, increased range of motion due to articulated Nguyen et al. conducted a review of 2804 laparoscopic liver resec-
instruments, recreating the seven-degrees of freedom of the hu- tions and found that 65 % of laparoscopic hepatectomies involve a
man wrist, leading to augmented surgical dexterity as well as im- non-anatomic resection or left lateral sectionectomy, while only
proved ergonomics due to a seated and comfortable operating 9 %, 7 %, and 1 % represent major anatomic right, major anatomic
position. These theoretical advantages of robotic surgery initiated left and extended hepatectomies, respectively [17]. These numbers
a broad utilization among various surgical specialties [6]. In Ger- call into question as to whether these more complex patients
many alone, the overall volume of robotic procedures rose from wouldn’t be the ones who profit the most from a minimal invasive
4 procedures in 2010 to 819 in 2015 [7]. While feasibility and safe- procedure, especially in terms of blood loss, post-operative recov-
ty of robotic surgery were clearly established by retrospective ery, cosmesis, pain, and length of stay [18]. Therefore, especially
case series and non-randomized data, subsequent randomized in complex cases including major hepatectomies, extended hepa-
control trials (RCTs) further demonstrated the non-inferiority of tectomies with biliary reconstruction and difficult segmentectom-
robotic surgery in oncological patients, including RCTs for bladder ies of the posterior-superior segments, robotic surgery appears to
cancer [8], rectal cancer [9], prostate cancer [10] or esophageal emerge as a reasonable alternative to open surgery rather than
cancer [11]. being an alternative to laparoscopic procedures.
Due to the theoretical advantages of the robotic assisted sys- In line with this Guerra et al. [19] promoted the uses of robotic
tem, complex liver surgery might be an especially interesting indi- surgery in resection of hepatic malignancies located in segment
cation for a robotic approach since it demands delicate tissue VII. While normally conducted by conventional open procedures
dissection (e. g. dissection of the hepatic hilum and hepatocaval with large thoracoabdominal or abdominal incisions [20], the ro-
plane or mobilization of the liver), precise intracorporeal suturing botic platform overcomes technical limitations of laparoscopic
(e. g. vascular reconstruction or biliary anastomosis) as well as surgery but retains the advantages of minimal invasive surgery,
difficult parenchymal transection with subsequent need for meti- including reduced trauma to the abdominal wall and parenchy-
culous hemostasis and biliostasis. This review will provide a gener- mal-sparing surgery [21]. Accordingly, Nota et al. [22] conducted
al overview of the existing literature along with current standards a multinational, multi-institutional propensity score-matched
and aims to specifically point out future directions of robotic liver study and reported superior short-term outcomes of robotic re-
surgery. sections of posterosuperior segments when compared to open
surgery. By further advancing the idea of specific patient selec-

Becker F et al. Robotic Liver Surgery… Z Gastroenterol 2021; 59: 56–62 | © 2020. Thieme. All rights reserved. 57
Übersicht

tion, Melstrom et al. developed a concept of selecting incision rate. When analyzing pooled data for postoperative outcome indi-
dominant cases for robotic liver surgery: They chose resections in cators, no significant differences were found. Guan et al. analyzed
poorly accessible locations, excluding a laparoscopic approach pooled data from 435 robotic and 503 laparoscopic cases and
and thus requiring large open incisions or cases in which the inci- found a significantly increased blood loss in the robotic cohort
sion was suggested to dominate the course of recovery [23]. By [37]. This is in contrast to recent meta-analyses by Kamarajah
employing this concept, they achieved a 90 % robotic completion et al., including 2630 patients (950 robotic and 1680 laparoscopic
rate and were able to discharge 66 % of all patients in less than cases) undergoing liver resection, revealing a significantly re-
three days (including three hemi-hepatectomies), with fourteen duced estimated blood loss with no differences in transfusion
patients even being discharged at the day of surgery. rates between robotic and laparoscopic liver resection [31].
Among the possible explanations for the apparently conflicting
Short-Term Outcomes finding regarding intraoperative blood loss is the mixed popula-
Due to paucity of RCTs, most data are drawn from single center tion of major and minor resections, with a trend to more extensive
case-cohort studies. The first large series was presented by Tsung resections in the robotic cohorts. When comparing only major
et al. in 2014 as a retrospective cohort study, matching 57 resection (removal of three or more Couinaud segments) be-
(36 minor, 21 major) robotic with 114 (72 minor, 42 major) tween 300 laparoscopic and 225 robotic cases, a recent meta-
laparoscopic (total, hand-assist and hybrid approaches) hepatic analysis by Ziogas et al. found no significant differences regarding
resections [18]. Parenchymal dissection was conducted by crush- transfusion rate and estimated blood loss, along with of overall
clamping techniques with clips and suturing for robotic resec- equal rates for severe complication and overall mortality [38].
tions, while linear staplers were used for laparoscopic liver resec- Therefore, it can be concluded that robotic and laparoscopic he-
tions. The authors found no significant differences in most opera- patectomy are equivalent regarding the majority of outcomes of

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tive (blood loss, transfusion rate), postoperative (postoperative interest.
peak bilirubin, postoperative intensive care unit admission rate,
length of stay and 90-day mortality, postoperative complications) Enhanced Recovery. A Key Step in Reducing Cost
as well as oncologic (R0 negative margin rate) outcomes. How- and Improving Oncological Outcomes
ever, a significant longer overall room time and OR time was no- The aspect of postoperative recovery has been studied by Frus-
ted in the robotic group. One interesting finding was that there cione et al. in a cohort of major liver resections (57 robotic and
were only four conversions to an open procedure in the robotic 116 laparoscopic). Among the key findings in this study are a sig-
group (bleeding, difficulty in liver mobilization and inability to nificantly reduced postoperative intensive care unit admission and
access hilum), demonstrating that 93 % of all robotic cases were 90-day readmission rates in the robotic group [29]. This was fur-
done purely minimally invasive. On the contrary, only 49.1 % of ther supported by a report from Cortolillo et al. [30] using large
laparoscopic cases were conducted in a purely minimally invasive registry data from the Nationwide Readmission Database. Com-
manner, with 10 conversions, 31 hand-assist procedures and pared to open (n = 10 146) and laparoscopic (n = 520) hepatect-
16 hybrid operations. When compared to open major hepatec- omy, robotic procedures (n = 204) were associated with a shorter
tomies, robotic surgery revealed a significantly reduced estimated length of stay and less frequent non-elective readmission within
blood loss and shorter hospital stay. This highlights that robotic 45 days. Same results were reported in two recent meta-analyses
surgery inherences the advantages of minimal invasive surgery by Kamarajah et al. as well as by Gavriilidis et al. revealing signifi-
over conventional procedures but might allow to perform more cantly lower readmission rate for robotic compared with laparo-
difficult and challenging procedures purely minimally invasive scopic liver resections [13, 31]. All of this provide evidence of
when compared to laparoscopic surgery. favorable recovery in patients undergoing robotic liver resection
With the absence of RCTs, the currently highest level of evi- as evident by reduced complications, lower rates of intensive
dence concerning robotic liver surgery can be drawn from meta care unit admissions, shorter length of stay and less frequent
analyses. Several meta-analyses have established that compared non-elective readmissions. This is of special interest for patients
with open hepatectomy robotic liver surgery is associated with with hepatic malignancies, since postoperative complications
significantly lower complications, reduced blood loss and blood have been shown negatively affect long-term survival and recur-
transfusion rates along with shorter length of stay, while provid- rence, while prolonged recovery expands the time to initiation of
ing similar R0 resection rates as well as equal rates for 5-year over- adjuvant chemotherapy, which has also negative effects on survi-
all and disease-free survival [13, 34–36]. val [32, 33]. This further emphazise theoretical advantages of
It is notable that the pooled data from meta-analyses compar- robotic surgery in patients with hepatic malignancies.
ing robotic with laparoscopic surgery are currently inconsistent.
Among the most recent meta-analysis is the work from Zhang Oncological Outcomes
et al., combining data from 28 articles, involving 3544 patients Having established safety and feasibility of robotic liver resection,
and comparing outcomes of robotic (1312 cases) with laparo- oncological outcomes became a special area of interest. A large
scopic (2232 cases) liver resection. The authors could demon- European bi-institutional study compared outcomes of liver resec-
strate that robotic liver surgery was associated with a longer op- tions for hepato-biliary malignancies between 111 laparoscopic
erative time, higher transfusion rate (although estimated blood with 61 robotic procedures in a propensity score matched study,
loss was equal between the two groups) but lower conversion with data being retrieved from prospectively maintained files

58 Becker F et al. Robotic Liver Surgery… Z Gastroenterol 2021; 59: 56–62 | © 2020. Thieme. All rights reserved.
[24]. The authors found no significant differences in operative tectomy plus caudate lobectomy or trisectionectomy, extrahepa-
time, blood transfusion as well as 90-day overall morbidity. A spe- tic bile duct resection, radical lymphadenectomy and Roux-en-Y
cial focus of this study was oncological outcome, showing that R1 hepaticojejunostomy) were technical feasible (no conversion oc-
resection rate as well as mean surgical margin width were similar curred), surprisingly the oncological outcome was inferior in the
in both groups. In addition, 1-, 2-, and 3-year overall survival rates robotic group, evident by a shorter recurrence-free survival time
as well as 1-, 2-, and 3-year recurrence-free survival were similar (median 15.5, range 6–60 months, Log-rank p = 0.029). Why
between the laparoscopic and robotic cohort. This study demon- these patients had an inferior oncological outcome remains
strates that the excellent oncological results obtained with laparo- unclear but possible explanations can be hypothesized: At first,
scopic surgery can be preserved when applying robotic surgery. patients in the robotic group showed a higher postoperative mor-
There are currently two larger series investigating oncological bidity, which is known to negatively correlate with the oncological
outcomes in terms of resection margins, disease-free and overall outcome. Then, a high rate of peritoneal metastasis/implantation
survival for robotic surgery in patients with hepatocellular carci- (40 % of patients) as well as multi-site metastasis (20 %) was nota-
noma. Chen et al. conducted a matched comparison between ro- ble, suggesting a possible implantation during surgery due to
botic and open hepatectomies, with 81 patients in each group instrumental manipulation or aerosols produced by power equip-
being compared under propensity score matching [27]. Percen- ped instruments. In addition, the robotic operations were con-
tage of major liver resections (41.9 for robotic vs. 39.5 % for ducted between 2009 and 2012, being at the early phase of the
open surgery) and liver cirrhosis (45.7 for robotic vs. 46.9 % for learning curve of the respective surgeons, which might have a rel-
open surgery) was comparable between the two groups, respec- evant impact, too. However, so far, these concerns were not
tively. In addition, hepatitis profiles, preoperative liver function followed by subsequent studies and highlight the urgent need
tests, tumor size, cancer TNM stage, histology grade and tumor for prospective, randomized data.

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localization were also similar. Surgical outcomes were comparable
except a significant longer operation time for robotic procedures.
However, the robotic group also showed a significantly reduced Future perspectives
shorter hospital stay (7.5 vs. 10.1 days), and lower dosages of pa-
Robotic surgery is only in the beginning of its evolution. Purely
tient-controlled analgesia. Concerning oncological results, 3-year
based on its digital nature, the robotic system will undoubtably
overall survival (92.67 for robotic vs. 93.7 % for open surgery)
be at the center of future innovations in liver surgery. Technical
showed no differences while 3-year disease-free survival of the
advances will be further fueled by completion as intellectual prop-
open group was markedly reduced (72.2 % for robotic vs. 58.0 for
erty constraints are fading and new companies are entering the
open surgery) without reaching statistical significance (p = 0.062).
market [39]. We can expect better systems for single-incision ro-
The largest series comparing long-term oncological outcomes of
botic surgery, which can be combined with natural orifice speci-
robotic (n = 100) and laparoscopic (n = 35) hepatectomies for he-
men extraction [40]. In addition, advances in parenchymal dissec-
patocellular carcinoma was published by Lai et al. [28]. Although
tion deceives such as a Cavitron Ultrasonic Surgical Aspirator
the robotic cohort had a significant higher proportion of major
(CUSA) for the robotic platform are urgently awaited. But we are
hepatectomies (27 % vs. 2.9 %) and tumors located at or across
also on the verge of a technical revolution, including upcoming of
posterosuperior segments (29 % vs. 0 %), morbidity and mortality
leverage integrated sensors, “smart instruments”, big data and
were comparable. Regarding oncological outcomes, the study
deep-learning technologies [39]. As of today, the robotic platform
showed similar results for R0 resection rates, 5-year overall survi-
already allows for integration of new technologies, including
val (65 % vs. 48 %), and disease-free survival (42 % vs. 38 %) be-
ultrasound instruments or indocyanine green imaging [41]. All of
tween robotic and laparoscopic groups. All together these studies
this will be further developed into augmented reality, providing
demonstrate a non-inferiority of robotic liver surgery for hepato-
the robotic surgeon with simultaneously displayed data and pa-
cellular carcinoma in terms of resection margins, disease-free and
tient-specific anatomical virtual models, allowing patient and
overall survival, while providing evidence for an enhanced post-
case specific image-guided surgery [42]. Future robotic platforms
operative patient recovery.
will provide more than technical refinements such as suppressing
The issue of oncological outcomes was further addressed by an
tremor, they will become more than a surgical tool by advancing
international, multicenter, retrospective study of 61 patients un-
torwards a learning, globally connected data-harvesting surgical
dergoing robotic liver surgery for hepatocellular carcinoma
interface. As a second level (parallel to pure technical support in
(56 %), cholangiocarcinoma (26 %) or gallbladder cancer (18 %)
a master-slave setup), robots will use algorithms based on biologi-
[25]. It was revealed 5-year overall- and disease-free survival
cal, technical and procedural data to offer intellectual support in
were 56 and 38 %, respectively, which is comparable to published
cyber-physical systems [39].
survival data for open and laparoscopic procedures. However,
In parallel to technical advances, robotic surgery will be used
subgroup analysis revealed inferior outcomes for patients with
for more complex operation in the future. In line with this, there
extrahepatic cholangiocarcinoma undergoing robotic liver sur-
are first reports about robotic associating liver partition and portal
gery. This was also postulated by Xu et al. [26] analyzing oncolo-
vein ligation for staged hepatectomy with excellent results in
gical outcomes of patients with hilar cholangiocarcinoma, of
highly selected cases [43–45].
which 10 (Bismuth–Corlette type II (n = 1), IIIa (n = 4), IIIb (n = 1)
In the setting of liver transplantation, robotic surgery can be
and IV (n = 4)) underwent robotic and 32 conventional open sur-
theoretically applied to live donor organ retrieval as well as the re-
gery. While these challenging robotic procedures (hemi-hepa-

Becker F et al. Robotic Liver Surgery… Z Gastroenterol 2021; 59: 56–62 | © 2020. Thieme. All rights reserved. 59
Übersicht

cipient operation. While living adult-to-adult as well as adult‐to‐ surgery compared to laparoscopic surgery (even for highly com-
pediatric liver transplantation are both considered a valuable plex cases), which will have a great impact on future results. This
approach to overcome organ shortage, the donor procedure will also be a factor when considering the two currently largest
demands the highest level of safety but at the time aims to main- disadvantages of robotic surgery, cost and operation time.
tain the donor’s quality of life. These two principal goals have Numerous studies now demonstrated a reduced overall cost due
driven the development of laparoscopic procedures and have to shorter ICU stay, shorter hospital and reduced readmissions.
encouraged the implication of robotic surgery to further reduce It is now thoroughly established that robotic liver surgery is
procedure associated mortality and morbidity in the donor. The safe and feasible compared to open and laparoscopic surgery,
first reported case of a robotic live donor right hepatectomy was with at least non-inferior oncological outcomes. It will be among
presented in 2012 by Giulianotti et al. followed a subsequent case the great challenges for the current and upcoming generation of
series, providing first evidence regarding feasibility and safety [46, robotic liver surgeons to identify patients who profit the most
47]. In 2020 Rho et al. [48] reported short-term outcomes from a from this technology, while at the same time accept and maybe
large Korean cohort study comparing robotic living donor right overcome current limitations in extended oncological resections.
hepatectomy with laparoscopy-assisted and conventional open However, the authors strongly believe that equal R0 rates and
donor right hepatectomy. While no differences were noted for identical lymph node rates in combination with parenchymal
postoperative complications, the robotic approach resulted in sparing resection, reduced blood loss, reduced trauma and
less blood loss and lower postoperative pain scores compared enhanced recovery will translate into superior oncological results
with the open procedure as well as better donor satisfaction with in future trials evaluating robotic liver surgery.
cosmetic results and body image when compared with the laparo-
scopic procedure. These results were confirmed by Broering et al. Conflict of Interest

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in a series 263 consecutive adult patients undergoing right lobe
living donor hepatectomy, of which 35 robotic and 70 open pro- The authors declare that they have no conflict of interest.
cedures were included in a propensity score matched analysis
[49]. The safety (no conversion, all grafts successfully transplan- References
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