- Email: [email protected]
Operative techniques to avoid near misses during laparoscopic hepatectomy
ARTICLE IN PRESS
Operative techniques to avoid near misses during laparoscopic hepatectomy Yoshikuni Kawaguchi, MD, PhD,a,b Vimalraj Velayutham, MD,a David Fuks, MD, PhD,a,c Frederic Mal, MD,a Norihiro Kokudo, MD, PhD,b and Brice Gayet, MD, PhD,a,c Paris, France, and Tokyo, Japan
Background. The lack of a complete hepatic overview and tactile feedback during laparoscopic hepatectomy may result in near misses or fatal intraoperative complications despite the advantage of a magnified laparoscopic view. The aim of the study is to describe operative techniques and guiding principles with which to address near misses unique to laparoscopic hepatectomy and evaluate the intraoperative complication rate overtime. Methods. Data of 408 consecutive patients who underwent laparoscopic hepatectomy were reviewed. Representative operative techniques and guiding principles with which to address near misses and pitfalls unique to laparoscopic hepatectomy were evaluated among the patients by 2 surgeons. Results. Most near misses were due to lack of understanding of both the laparoscopic view and anatomic aspects unique to laparoscopic hepatectomy. Operative techniques and/or guiding principles with which to address these issues were demonstrated as follows: starting parenchymal transection at the declivitous parts; no ligation of the right or left portal vein before confirming the bifurcation; dissection of the short hepatic vein using a sealing device; dissection of the root of the hepatic vein using scissors; exposure of the middle hepatic vein, which is anatomically close to the hilar plate; and identification of V8 using intraoperative ultrasonography. The intraoperative massive bleeding due to vessel injury or surgical clip slippage occurred in 25 patients (6.1%), and its rate had a significant trend to decrease with increasing years. Conclusion. We demonstrated operative techniques and guiding principles with which to address near misses in laparoscopic hepatectomy. The intraoperative massive bleeding rate trended to decrease over time. (Surgery 2016;j:j-j.) From the Department of Digestive Diseases,a Institut Mutualiste Montsouris, Universite Paris Descartes, Paris, France; the Hepato-Biliary-Pancreatic Surgery Division, Department of Surgery,b Graduate School of Medicine, University of Tokyo, Tokyo, Japan; and the Institut des Syste mes Intelligents et Robotique,c Universite Pierre et Marie Curie, Paris, France
LAPAROSCOPIC HEPATECTOMY (LH) has increasingly gained popularity throughout the world.1-6 According to recent reviews of world literature,7,8 LH is associated with less blood loss and lower postoperative morbidity than is open hepatectomy with no significant difference in oncologic outcomes. These results are conceivably due to the advantages of laparoscopic approach, which allows for The authors declare that they have no conflict of interest. Accepted for publication July 14, 2016. Reprint requests: Brice Gayet, MD, PhD, and Yoshikuni Kawaguchi, MD, PhD, Department of Digestive Diseases, Institut Mutualiste Montsouris, Universite Paris Descartes, 42 boulevard Jourdan, 75014 Paris, France. E-mail: yokawaguchi-tky@umin. ac.jp or [email protected]. 0039-6060/$ - see front matter Ó 2016 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.surg.2016.07.023
a magnified view,9,10 and the hemostatic effect caused by pneumoperitoneum.11 In contrast, potential disadvantages of LH are the lack of both complete hepatic view and tactile feedback,12 which may mislead surgeons into near misses or fatal intraoperative complications. Operative techniques and/or guiding principles for LH are required to compensate for these disadvantages and avoid near misses during LH. However, no published series have focused on those techniques. Thus, the operative techniques with which to avoid near misses and pitfalls during LH remain unclear. In our institution, the operative techniques of LH have been innovated and modified over time. These experiences have improved our understanding of the laparoscopic view, which lacks a sufficiently complete hepatic view compared with the magnified view, and the anatomic aspects unique to LH. The aim of this study was to demonstrate the near misses SURGERY 1
ARTICLE IN PRESS 2 Kawaguchi et al
and pitfalls unique to LH and illustrate the operative techniques and guiding principles with which to address them in accompanying videos. METHODS Patients. From 2001 to 2012, 408 consecutive patients underwent LH by a single surgeon (BG) at the Institut Mutualiste Montsouris, Universit e Paris Descartes. Representative operative techniques and guiding principles with which to address near misses and pitfalls unique to LH were evaluated among the patients by 2 surgeons (YK and BG). The clinical records of these patients were retrospectively reviewed from a prospectively maintained database. All operations were performed after obtaining informed consent from each patient. The local institutional review board approved this study. Basic operative techniques. Our basic techniques of LH have been described elsewhere.1,13,14 Briefly, the patients were placed in the low lithotomy position, with the legs spread apart and bent at the knees (French position). A 12-mm trocar was placed high at the right hypochondrium for intraoperative ultrasonography and vascular stapling. Three or 4 additional 5-mm operative ports were also placed. Intermittent inflow occlusion (Pringle maneuver15) was used only in cases of massive and/or persistent bleeding. Parenchymal transection was performed using a bipolar forceps (Micro France CEV134; Medtronic, Minneapolis, MN) and ultrasonic laparoscopic coagulation shears (SonoSurg; Olympus Co, Tokyo, Japan) or an ultrasonic cutting and coagulating device (THUNDERBEAT; Olympus Co). The hepatic vessels were divided using a sealing device or endoscopic clips (Hem-o-Lok clip; Weck Surgical Instruments, Research Triangle Park, NC) depending on their diameter. After parenchymal transection, the resected specimen was placed in a plastic bag and retrieved unfragmented through a small incision normally made on the lower abdomen. Drains were placed only if there was concern about an increased risk of postoperative bleeding and bile leakage. Major hepatectomy is defined as the resection of $3 contiguous segments according to Couinaud.16 Morbidity and mortality were respectively defined as postoperative complications and death within 90 days after an operation. Evaluation of intraoperative massive bleeding. Intraoperative massive bleeding in our study was defined as bleeding caused by injury to vessels or slippage of the surgical clip during LH with total estimated blood loss >1,000 mL. The proportion
Surgery j 2016
of intraoperative massive bleeding was assessed by each year. Statistical analysis. Categorical variables are expressed in numerical figures and percentages. Continuous variables were expressed as median values (with the range). The trends of intraoperative complication rates with a stepwise increase from 2001 to 2012 were evaluated using the JonckheereTerpstra trend test.17 Statistical analysis was conducted with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphic user interface for R software (The R Foundation for Statistical Computing, Vienna, Austria).18 RESULTS Operative techniques and guiding principles with which to address near misses unique to LH. The operative techniques and guiding principles with which to address near misses and pitfalls unique to LH were divided into 6 parts as follows: Start of parenchymal transection at the declivitous parts of the liver when performing wedge resection. Parenchymal transection should be started at the declivitous parts of the liver for any wedge resection (Fig 1). This principle ensures parenchymal transection of the upper part of the liver without oozing after bleeding control in the lower part of the liver. Blood would trickle from the upper to the lower part of the liver if parenchymal transection was started from the acclivitous part of the liver. Such trickling blood at the upper part interferes with subsequent parenchymal transection of the lower part of the liver, causing increased blood loss and prolonged transection (Supplementary Video 1). Confirmation of the portal vein bifurcation. The right or left portal vein must not be ligated before confirming the portal vein bifurcation. Especially during right hemi-hepatectomy, misidentification of the right portal vein as the main portal vein must be avoided. The magnified view sufficiently lacks complete hepatic view, possibly leading to such misidentification; this may be a fatal error for patients, as representatively shown in Fig 2 and Supplementary Video 2. Sealing the short hepatic vein especially at the lower part of the inferior vena cava. A sealing device is useful to dissect the short hepatic vein, especially at the lower part of the inferior vena cava (IVC). When ligating the short hepatic vein on IVC, attention must be paid to the potential risk of surgical clip slippage. These clips are located outside the viewing field of the laparoscope during parenchymal transection at the upper level of the liver. Contact with forceps unintentionally causes
ARTICLE IN PRESS Surgery Volume j, Number j
Kawaguchi et al 3
Fig 1. The declivitous (arrowheads) and acclivitous (arrow) parts of the liver are shown in the laparoscopic view (left). Parenchymal transection of wedge resection was started from the declivitous part of the liver (right). (Color version of this figure is available online.)
slipping of the clips from the stump of the IVC, potentially resulting in fatal bleeding. Before sealing the short hepatic veins, we coagulated them using bipolar forceps as shown in Supplementary Video 3. Sealing is subsequently performed when the vessels shrink. Otherwise, surgical clips are used for the vessels. We have not yet experienced bleeding from the stump of the IVC following these steps. Dissection of the root of the hepatic vein. Laparoscopic scissors should be used when parenchymal transection comes close to the posterior capsule of the liver. With cautious dissection using scissors, injury to the IVC and/or root of the hepatic vein will either not occur or be minimized to small holes. Dissection using energy devices creates larger holes on vessels than dissection with scissors does and potentially causes massive bleeding from the vessels (Supplementary Video 4). Exposure of the middle hepatic vein during parenchymal transection. Transection of the liver parenchyma above the hilar plate from the caudate side must be cautiously performed before exposure of the middle hepatic vein (MHV) or its branch to avoid injury to the MHV. The peripheral part of the MHV is generally identified close to the hilar plate. Attention must be paid to the MHV, which may be the source of massive bleeding during left or right hemi-hepatectomy. At our institution, the major hepatic vein is exposed on the raw surface during major hepatectomy because its exposure not only enables accurate anatomic resection, improving the oncologic outcome in the treatment of hepatocellular carcinoma,19,20 but also serves as the anatomic landmark for the direction of transection.
When parenchymal transection during left hepatectomy is started from the caudate side of the liver after division of the left hepatic vessels, the MHV is identified approximately 1 cm away from the hilar plate (Fig 3 and Supplementary Video 5). When performing parenchymal transection during right hepatectomy from the caudate side of the liver, the branch of the MHV in segment V (V5) is usually identified within 1 cm of the hilar plate. After ligation and division of V5 and subsequent transection, the MHV is also identified approximately 1 cm away from the hilar plate as in left hepatectomy (Fig 3 and Supplementary Video 6). Branch of the MHV from segment VIII (V8). V8 must be identified and confirmed using intraoperative ultrasonography to avoid its injury. A difficult-torecognize error during laparoscopic right hepatectomy is injury to V8. Tearing between V8 and the MHV causes massive bleeding because V8 is closer to the IVC than are other branches of the MHV. Thus, bleeding at this point is comparable with that at the IVC itself and must be avoided (Fig 4 and Supplementary Video 7). Patient characteristics. Of 408 patients, 246 were men (60.2%) and 162 were women (39.8%), with a median age of 63 (range, 18–89) years, median body mass index of 25.3 (range, 15.4–35.7) kg/m2, and median American Society of Anesthesiologists classification of 2 (range, 1–3). A total of 162 (39.7%) patients had $1 comorbidity, and 178 (43.6%) had undergone chemotherapy, including 155 oxaliplatin-based regimens. Intraoperative outcomes. Median estimated blood loss was 150 mL (range 0–4,500 mL), and median operation time was 200 minutes (range 40–720 minutes). The transfusion rate was 5.9%.
ARTICLE IN PRESS 4 Kawaguchi et al
Fig 2. (A) Operative view of hepatic portal region through a laparoscope shows the portal vein, namely the “right” portal vein (arrowheads), common hepatic duct (white arrow), and right hepatic artery (white arrowhead). (B) After ligation and division of the right hepatic artery (white arrowhead), subsequent dissection along the portal vein (arrowheads) on the right side of the common bile duct (white arrow) reveals its branch into the right liver (posterior right portal vein, arrow). (C) After identification of the left portal vein (white arrowheads), the last branch into the right liver (anterior right portal vein, white arrow) was ligated: the main portal vein (arrowhead) and the stump of the posterior right portal vein (arrow). (Color version of this figure is available online.)
Surgery j 2016
Fig 3. (A) Laparoscopic operative view from the caudal side of the liver during left hemi-hepatectomy. The middle hepatic vein (arrowheads) is visualized close to the hepatoduodenal ligament (white arrowheads): the stump of the left hepatic duct (arrow). (B) Laparoscopic operative view from the caudal side of the liver during right hemi-hepatectomy. The middle hepatic vein (arrowheads) is visualized close to the hepatoduodenal ligament (white arrowheads): the stump of the right hepatic duct (arrow). (Color version of this figure is available online.)
The majority (368 patients, 90.2%) underwent LH for malignancy and 40 for a benign indication (9.8%). Laparoscopic major hepatectomy was performed in 155 patients (38.0%). The proportion of major hepatectomy increased from 33.8% (2001– 2007) to 40.4% (2008–2012), without a significant difference (P = .187). Intraoperative massive bleeding occurred in 25 patients (6.1%). Intraoperative massive bleeding rates had a significant trend to decrease with increasing years, from
ARTICLE IN PRESS Surgery Volume j, Number j
Kawaguchi et al 5
Fig 5. Intraoperative complication rates show a significant trend to decrease with increasing years, from 2001 to 2012 (Jonckheere-Terpstra trend test, P < .021). Fig 4. After the first half of parenchymal transection along with the middle hepatic vein, a branch of the middle hepatic vein from segment VIII (V8) (arrowheads) is identified and confirmed using intraoperative ultrasound, which visualizes the conjunction between V8 and the middle hepatic vein close to the inferior vena cava (arrow). (Color version of this figure is available online.)
2001 to 2012 (Jonckheere-Terpstra trend test, P < .021) (Fig 5). The rate of conversion to open approach was 5.9%. Postoperative outcomes. The postoperative mortality and postoperative morbidity rates were 1.1 % and 32.9 %, respectively. Fifty-four patients (12.3 %) developed complications graded in Clavien-Dindo classification21 III and IV. DISCUSSION Our study results and accompanying videos demonstrate the near misses and pitfalls that may be encountered during LH and the operative techniques and guiding principles with which to address them. Most near misses were caused by a lack of understanding of both the laparoscopic view of the liver (operative techniques 1, 2, and 3) and anatomic aspects (operative techniques 5 and 6) unique to LH. These techniques and principles have been modified throughout our experience, which has revealed a wide variety of near misses and pitfalls during LH. Intraoperative complication rates at our institute trended to decrease from 2001 to 2012 (Fig 5), while operative procedures shifted to include more major laparoscopic hepatectomy over time. Chronologic improvements of operative techniques for LH, as in the decreasing trend of intraoperative complication rates, can generally be explained by the learning curve.22,23 However,
such an explanation might encourage surgeons to steadily and gradually perform LH. We sought to demonstrate the components hidden in the learning curve in clinical practice or, in other words, the gap between beginners and experts, focusing on near misses and pitfalls during LH and proposing techniques and principles with which to avoid them. These techniques and principles have guided us to avoid critical pitfalls and near misses during LH and have decreased the intraoperative complication rates at our institution. The magnified views unique to laparoscopic surgery are recognized as a potential advantage over open surgery.9,10 The laparoscopic up-view from the caudal side provides a better operative view behind the liver or around the IVC than does open hepatectomy. However, any surgeon who performs LH must remember that the magnified laparoscopic view itself may ironically mislead surgeons, resulting in critical misjudgments or errors because of the lack of a complete hepatic overview, as demonstrated in Supplementary Videos 2 and 3. In fact, massive bleeding associated with vessel injury or surgical clip slippage (6.1%) occurred due in part to the lack of a hepatic overview. The laparoscopic view from the caudal side of the liver facilitates parenchymal transection during LH. However, it potentially causes injury to the MHV when surgeons lack the anatomic understanding unique to the LH, specifically that the peripheral branch of the MHV is located in close proximity to the hilar plate, as representatively demonstrated in Supplementary Videos 5 and 6. In addition to an understanding of the laparoscopic view and anatomic aspects unique to LH, a systematic technique of intraoperative ultrasonography is helpful for surgeons to avoid
ARTICLE IN PRESS 6 Kawaguchi et al
injury to the hepatic vessels.24 The technologic innovations, such as three-dimensional video systems,25 laparoscopic intraoperative ultrasonography with contrast agents,26 real-time tissue elastography,12 and indocyanine green-fluorescence imaging technique,27 have helped surgeons identify the anatomic structure of the liver. We believe that the techniques and principles demonstrated in the present study are also helpful for surgeons who perform LH. They have developed over a single surgeon’s experiences, however, and therefore need to be addressed by other groups. An increasing number of reports on potential near misses and their solutions are essential to further improve the safety of LH, not to mention a prospective and multicenter approach to minimize intraoperative complications. In conclusion, we have demonstrated the operative techniques and guiding principles with which to address near misses and pitfalls of LH, which are due in large part to the disadvantage of the laparoscopic magnified view and the lack of understanding of the anatomic aspects unique to LH. These techniques and principles are expected to help surgeons to avoid intraoperative complications and ensure the safety of LH. The authors thank Takeo Nomi for coordinating the patients’ follow-up and maintaining the prospective database that formed the basis of this study. SUPPLEMENTARY DATA Supplementary data related to this article can be found online at http://dx.doi.org/10.1016/j.surg.2016.07.023.
REFERENCES 1. Vibert E, Perniceni T, Levard H, Denet C, Shahri NK, Gayet B. Laparoscopic liver resection. Br J Surg 2006;93:67-72. 2. Otsuka Y, Tsuchiya M, Maeda T, Katagiri T, Isii J, Tamura A, et al. Laparoscopic hepatectomy for liver tumors: proposals for standardization. J Hepatobiliary Pancreat Surg 2009;16:720-5. 3. Nitta H, Sasaki A, Fujita T, Itabashi H, Hoshikawa K, Takahara T, et al. Laparoscopy-assisted major liver resections employing a hanging technique: the original procedure. Ann Surg 2010;251:450-3. 4. Nguyen KT, Marsh JW, Tsung A, Steel JJ, Gamblin TC, Geller DA. Comparative benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg 2011;146:348-56. 5. Cannon RM, Brock GN, Marvin MR, Buell JF. Laparoscopic liver resection: an examination of our first 300 patients. J Am Coll Surg 2011;213:501-7. 6. Hwang DW, Han HS, Yoon YS, Cho JY, Kwon Y, Kim JH, et al. Laparoscopic major liver resection in Korea: a multicenter study. J Hepatobiliary Pancreat Sci 2013;20:125-30. 7. Croome KP, Yamashita MH. Laparoscopic vs open hepatic resection for benign and malignant tumors: An updated meta-analysis. Arch Surg 2010;145:1109-18.
Surgery j 2016
8. Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2,804 patients. Ann Surg 2009;250:831-41. 9. Hoznek A, Salomon L, Olsson LE, Antiphon P, Saint F, Cicco A, et al. Laparoscopic radical prostatectomy. The Creteil experience. Eur Urol 2001;40:38-45. 10. Asoglu O, Matlim T, Karanlik H, Atar M, Muslumanoglu M, Kapran Y, et al. Impact of laparoscopic surgery on bladder and sexual function after total mesorectal excision for rectal cancer. Surg Endosc 2009;23:296-303. 11. Eiriksson K, Fors D, Rubertsson S, Arvidsson D. High intraabdominal pressure during experimental laparoscopic liver resection reduces bleeding but increases the risk of gas embolism. Br J Surg 2011;98:845-52. 12. Kawaguchi Y, Tanaka N, Nagai M, Nomura Y, Fuks D, Gayet B, et al. Usefulness of intraoperative real-time tissue elastography during laparoscopic hepatectomy. J Am Coll Surg 2015;221:e103-11. 13. Ishizawa T, Gumbs AA, Kokudo N, Gayet B. Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 2012;256:959-64. 14. Gumbs AA, Gayet B. Adopting Gayet’s techniques of totally laparoscopic liver surgery in the United States. Liver Cancer 2013;2:5-15. 15. Pringle JH. V. Notes on the arrest of hepatic hemorrhage due to trauma. Ann Surg 1908;48:541-9. 16. Couinaud C. Surgical anatomy of the liver revisited. Paris: C. Couinaud; 1989. 17. Mikami S, Hamano T, Fujii N, Nagasawa Y, Isaka Y, Moriyama T, et al. Serum osteoprotegerin as a screening tool for coronary artery calcification score in diabetic predialysis patients. Hypertens Res 2008;31:1163-70. 18. Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 2013;48:452-8. 19. Eguchi S, Kanematsu T, Arii S, Okazaki M, Okita K, Omata M, et al. Comparison of the outcomes between an anatomical subsegmentectomy and a non-anatomical minor hepatectomy for single hepatocellular carcinomas based on a Japanese nationwide survey. Surgery 2008;143:469-75. 20. Hasegawa K, Kokudo N, Imamura H, Matsuyama Y, Aoki T, Minagawa M, et al. Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg 2005;242:252-9. 21. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 2009;250:187-96. 22. Cai X, Li Z, Zhang Y, Yu H, Liang X, Jin R, et al. Laparoscopic liver resection and the learning curve: a 14-year, single-center experience. Surg Endosc 2014;28:1334-41. 23. Vigano L, Laurent A, Tayar C, Tomatis M, Ponti A, Cherqui D. The learning curve in laparoscopic liver resection: improved feasibility and reproducibility. Ann Surg 2009;250:772-82. 24. Araki K, Conrad C, Ogiso S, Kuwano H, Gayet B. Intraoperative ultrasonography of laparoscopic hepatectomy: key technique for safe liver transection. J Am Coll Surg 2014;218:e37-41. 25. Storz P, Buess GF, Kunert W, Kirschniak A. 3D HD versus 2D HD: surgical task efficiency in standardised phantom tasks. Surg Endosc 2012;26:1454-60. 26. Kawaguchi Y, Tanaka N, Kokudo N. Surgical value of contrast-enhanced ultrasonography in laparoscopic hepatectomy using energy devices. J Hepatobiliary Pancreat Sci 2014;21:78-9. 27. Kawaguchi Y, Velayutham V, Fuks D, Christidis C, Kokudo N, Gayet B. Usefulness of indocyanine green-fluorescence imaging for visualization of the bile duct during laparoscopic liver resection. J Am Coll Surg 2015;221:e113-7.
Operative techniques to avoid near misses during laparoscopic hepatectomy Yoshikuni Kawaguchi, MD, PhD,a,b Vimalraj Velayutham, MD,a David Fuks, MD, PhD,a,c Frederic Mal, MD,a Norihiro Kokudo, MD, PhD,b and Brice Gayet, MD, PhD,a,c Paris, France, and Tokyo, Japan
Background. The lack of a complete hepatic overview and tactile feedback during laparoscopic hepatectomy may result in near misses or fatal intraoperative complications despite the advantage of a magnified laparoscopic view. The aim of the study is to describe operative techniques and guiding principles with which to address near misses unique to laparoscopic hepatectomy and evaluate the intraoperative complication rate overtime. Methods. Data of 408 consecutive patients who underwent laparoscopic hepatectomy were reviewed. Representative operative techniques and guiding principles with which to address near misses and pitfalls unique to laparoscopic hepatectomy were evaluated among the patients by 2 surgeons. Results. Most near misses were due to lack of understanding of both the laparoscopic view and anatomic aspects unique to laparoscopic hepatectomy. Operative techniques and/or guiding principles with which to address these issues were demonstrated as follows: starting parenchymal transection at the declivitous parts; no ligation of the right or left portal vein before confirming the bifurcation; dissection of the short hepatic vein using a sealing device; dissection of the root of the hepatic vein using scissors; exposure of the middle hepatic vein, which is anatomically close to the hilar plate; and identification of V8 using intraoperative ultrasonography. The intraoperative massive bleeding due to vessel injury or surgical clip slippage occurred in 25 patients (6.1%), and its rate had a significant trend to decrease with increasing years. Conclusion. We demonstrated operative techniques and guiding principles with which to address near misses in laparoscopic hepatectomy. The intraoperative massive bleeding rate trended to decrease over time. (Surgery 2016;j:j-j.) From the Department of Digestive Diseases,a Institut Mutualiste Montsouris, Universite Paris Descartes, Paris, France; the Hepato-Biliary-Pancreatic Surgery Division, Department of Surgery,b Graduate School of Medicine, University of Tokyo, Tokyo, Japan; and the Institut des Syste mes Intelligents et Robotique,c Universite Pierre et Marie Curie, Paris, France
LAPAROSCOPIC HEPATECTOMY (LH) has increasingly gained popularity throughout the world.1-6 According to recent reviews of world literature,7,8 LH is associated with less blood loss and lower postoperative morbidity than is open hepatectomy with no significant difference in oncologic outcomes. These results are conceivably due to the advantages of laparoscopic approach, which allows for The authors declare that they have no conflict of interest. Accepted for publication July 14, 2016. Reprint requests: Brice Gayet, MD, PhD, and Yoshikuni Kawaguchi, MD, PhD, Department of Digestive Diseases, Institut Mutualiste Montsouris, Universite Paris Descartes, 42 boulevard Jourdan, 75014 Paris, France. E-mail: yokawaguchi-tky@umin. ac.jp or [email protected]. 0039-6060/$ - see front matter Ó 2016 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.surg.2016.07.023
a magnified view,9,10 and the hemostatic effect caused by pneumoperitoneum.11 In contrast, potential disadvantages of LH are the lack of both complete hepatic view and tactile feedback,12 which may mislead surgeons into near misses or fatal intraoperative complications. Operative techniques and/or guiding principles for LH are required to compensate for these disadvantages and avoid near misses during LH. However, no published series have focused on those techniques. Thus, the operative techniques with which to avoid near misses and pitfalls during LH remain unclear. In our institution, the operative techniques of LH have been innovated and modified over time. These experiences have improved our understanding of the laparoscopic view, which lacks a sufficiently complete hepatic view compared with the magnified view, and the anatomic aspects unique to LH. The aim of this study was to demonstrate the near misses SURGERY 1
ARTICLE IN PRESS 2 Kawaguchi et al
and pitfalls unique to LH and illustrate the operative techniques and guiding principles with which to address them in accompanying videos. METHODS Patients. From 2001 to 2012, 408 consecutive patients underwent LH by a single surgeon (BG) at the Institut Mutualiste Montsouris, Universit e Paris Descartes. Representative operative techniques and guiding principles with which to address near misses and pitfalls unique to LH were evaluated among the patients by 2 surgeons (YK and BG). The clinical records of these patients were retrospectively reviewed from a prospectively maintained database. All operations were performed after obtaining informed consent from each patient. The local institutional review board approved this study. Basic operative techniques. Our basic techniques of LH have been described elsewhere.1,13,14 Briefly, the patients were placed in the low lithotomy position, with the legs spread apart and bent at the knees (French position). A 12-mm trocar was placed high at the right hypochondrium for intraoperative ultrasonography and vascular stapling. Three or 4 additional 5-mm operative ports were also placed. Intermittent inflow occlusion (Pringle maneuver15) was used only in cases of massive and/or persistent bleeding. Parenchymal transection was performed using a bipolar forceps (Micro France CEV134; Medtronic, Minneapolis, MN) and ultrasonic laparoscopic coagulation shears (SonoSurg; Olympus Co, Tokyo, Japan) or an ultrasonic cutting and coagulating device (THUNDERBEAT; Olympus Co). The hepatic vessels were divided using a sealing device or endoscopic clips (Hem-o-Lok clip; Weck Surgical Instruments, Research Triangle Park, NC) depending on their diameter. After parenchymal transection, the resected specimen was placed in a plastic bag and retrieved unfragmented through a small incision normally made on the lower abdomen. Drains were placed only if there was concern about an increased risk of postoperative bleeding and bile leakage. Major hepatectomy is defined as the resection of $3 contiguous segments according to Couinaud.16 Morbidity and mortality were respectively defined as postoperative complications and death within 90 days after an operation. Evaluation of intraoperative massive bleeding. Intraoperative massive bleeding in our study was defined as bleeding caused by injury to vessels or slippage of the surgical clip during LH with total estimated blood loss >1,000 mL. The proportion
Surgery j 2016
of intraoperative massive bleeding was assessed by each year. Statistical analysis. Categorical variables are expressed in numerical figures and percentages. Continuous variables were expressed as median values (with the range). The trends of intraoperative complication rates with a stepwise increase from 2001 to 2012 were evaluated using the JonckheereTerpstra trend test.17 Statistical analysis was conducted with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphic user interface for R software (The R Foundation for Statistical Computing, Vienna, Austria).18 RESULTS Operative techniques and guiding principles with which to address near misses unique to LH. The operative techniques and guiding principles with which to address near misses and pitfalls unique to LH were divided into 6 parts as follows: Start of parenchymal transection at the declivitous parts of the liver when performing wedge resection. Parenchymal transection should be started at the declivitous parts of the liver for any wedge resection (Fig 1). This principle ensures parenchymal transection of the upper part of the liver without oozing after bleeding control in the lower part of the liver. Blood would trickle from the upper to the lower part of the liver if parenchymal transection was started from the acclivitous part of the liver. Such trickling blood at the upper part interferes with subsequent parenchymal transection of the lower part of the liver, causing increased blood loss and prolonged transection (Supplementary Video 1). Confirmation of the portal vein bifurcation. The right or left portal vein must not be ligated before confirming the portal vein bifurcation. Especially during right hemi-hepatectomy, misidentification of the right portal vein as the main portal vein must be avoided. The magnified view sufficiently lacks complete hepatic view, possibly leading to such misidentification; this may be a fatal error for patients, as representatively shown in Fig 2 and Supplementary Video 2. Sealing the short hepatic vein especially at the lower part of the inferior vena cava. A sealing device is useful to dissect the short hepatic vein, especially at the lower part of the inferior vena cava (IVC). When ligating the short hepatic vein on IVC, attention must be paid to the potential risk of surgical clip slippage. These clips are located outside the viewing field of the laparoscope during parenchymal transection at the upper level of the liver. Contact with forceps unintentionally causes
ARTICLE IN PRESS Surgery Volume j, Number j
Kawaguchi et al 3
Fig 1. The declivitous (arrowheads) and acclivitous (arrow) parts of the liver are shown in the laparoscopic view (left). Parenchymal transection of wedge resection was started from the declivitous part of the liver (right). (Color version of this figure is available online.)
slipping of the clips from the stump of the IVC, potentially resulting in fatal bleeding. Before sealing the short hepatic veins, we coagulated them using bipolar forceps as shown in Supplementary Video 3. Sealing is subsequently performed when the vessels shrink. Otherwise, surgical clips are used for the vessels. We have not yet experienced bleeding from the stump of the IVC following these steps. Dissection of the root of the hepatic vein. Laparoscopic scissors should be used when parenchymal transection comes close to the posterior capsule of the liver. With cautious dissection using scissors, injury to the IVC and/or root of the hepatic vein will either not occur or be minimized to small holes. Dissection using energy devices creates larger holes on vessels than dissection with scissors does and potentially causes massive bleeding from the vessels (Supplementary Video 4). Exposure of the middle hepatic vein during parenchymal transection. Transection of the liver parenchyma above the hilar plate from the caudate side must be cautiously performed before exposure of the middle hepatic vein (MHV) or its branch to avoid injury to the MHV. The peripheral part of the MHV is generally identified close to the hilar plate. Attention must be paid to the MHV, which may be the source of massive bleeding during left or right hemi-hepatectomy. At our institution, the major hepatic vein is exposed on the raw surface during major hepatectomy because its exposure not only enables accurate anatomic resection, improving the oncologic outcome in the treatment of hepatocellular carcinoma,19,20 but also serves as the anatomic landmark for the direction of transection.
When parenchymal transection during left hepatectomy is started from the caudate side of the liver after division of the left hepatic vessels, the MHV is identified approximately 1 cm away from the hilar plate (Fig 3 and Supplementary Video 5). When performing parenchymal transection during right hepatectomy from the caudate side of the liver, the branch of the MHV in segment V (V5) is usually identified within 1 cm of the hilar plate. After ligation and division of V5 and subsequent transection, the MHV is also identified approximately 1 cm away from the hilar plate as in left hepatectomy (Fig 3 and Supplementary Video 6). Branch of the MHV from segment VIII (V8). V8 must be identified and confirmed using intraoperative ultrasonography to avoid its injury. A difficult-torecognize error during laparoscopic right hepatectomy is injury to V8. Tearing between V8 and the MHV causes massive bleeding because V8 is closer to the IVC than are other branches of the MHV. Thus, bleeding at this point is comparable with that at the IVC itself and must be avoided (Fig 4 and Supplementary Video 7). Patient characteristics. Of 408 patients, 246 were men (60.2%) and 162 were women (39.8%), with a median age of 63 (range, 18–89) years, median body mass index of 25.3 (range, 15.4–35.7) kg/m2, and median American Society of Anesthesiologists classification of 2 (range, 1–3). A total of 162 (39.7%) patients had $1 comorbidity, and 178 (43.6%) had undergone chemotherapy, including 155 oxaliplatin-based regimens. Intraoperative outcomes. Median estimated blood loss was 150 mL (range 0–4,500 mL), and median operation time was 200 minutes (range 40–720 minutes). The transfusion rate was 5.9%.
ARTICLE IN PRESS 4 Kawaguchi et al
Fig 2. (A) Operative view of hepatic portal region through a laparoscope shows the portal vein, namely the “right” portal vein (arrowheads), common hepatic duct (white arrow), and right hepatic artery (white arrowhead). (B) After ligation and division of the right hepatic artery (white arrowhead), subsequent dissection along the portal vein (arrowheads) on the right side of the common bile duct (white arrow) reveals its branch into the right liver (posterior right portal vein, arrow). (C) After identification of the left portal vein (white arrowheads), the last branch into the right liver (anterior right portal vein, white arrow) was ligated: the main portal vein (arrowhead) and the stump of the posterior right portal vein (arrow). (Color version of this figure is available online.)
Surgery j 2016
Fig 3. (A) Laparoscopic operative view from the caudal side of the liver during left hemi-hepatectomy. The middle hepatic vein (arrowheads) is visualized close to the hepatoduodenal ligament (white arrowheads): the stump of the left hepatic duct (arrow). (B) Laparoscopic operative view from the caudal side of the liver during right hemi-hepatectomy. The middle hepatic vein (arrowheads) is visualized close to the hepatoduodenal ligament (white arrowheads): the stump of the right hepatic duct (arrow). (Color version of this figure is available online.)
The majority (368 patients, 90.2%) underwent LH for malignancy and 40 for a benign indication (9.8%). Laparoscopic major hepatectomy was performed in 155 patients (38.0%). The proportion of major hepatectomy increased from 33.8% (2001– 2007) to 40.4% (2008–2012), without a significant difference (P = .187). Intraoperative massive bleeding occurred in 25 patients (6.1%). Intraoperative massive bleeding rates had a significant trend to decrease with increasing years, from
ARTICLE IN PRESS Surgery Volume j, Number j
Kawaguchi et al 5
Fig 5. Intraoperative complication rates show a significant trend to decrease with increasing years, from 2001 to 2012 (Jonckheere-Terpstra trend test, P < .021). Fig 4. After the first half of parenchymal transection along with the middle hepatic vein, a branch of the middle hepatic vein from segment VIII (V8) (arrowheads) is identified and confirmed using intraoperative ultrasound, which visualizes the conjunction between V8 and the middle hepatic vein close to the inferior vena cava (arrow). (Color version of this figure is available online.)
2001 to 2012 (Jonckheere-Terpstra trend test, P < .021) (Fig 5). The rate of conversion to open approach was 5.9%. Postoperative outcomes. The postoperative mortality and postoperative morbidity rates were 1.1 % and 32.9 %, respectively. Fifty-four patients (12.3 %) developed complications graded in Clavien-Dindo classification21 III and IV. DISCUSSION Our study results and accompanying videos demonstrate the near misses and pitfalls that may be encountered during LH and the operative techniques and guiding principles with which to address them. Most near misses were caused by a lack of understanding of both the laparoscopic view of the liver (operative techniques 1, 2, and 3) and anatomic aspects (operative techniques 5 and 6) unique to LH. These techniques and principles have been modified throughout our experience, which has revealed a wide variety of near misses and pitfalls during LH. Intraoperative complication rates at our institute trended to decrease from 2001 to 2012 (Fig 5), while operative procedures shifted to include more major laparoscopic hepatectomy over time. Chronologic improvements of operative techniques for LH, as in the decreasing trend of intraoperative complication rates, can generally be explained by the learning curve.22,23 However,
such an explanation might encourage surgeons to steadily and gradually perform LH. We sought to demonstrate the components hidden in the learning curve in clinical practice or, in other words, the gap between beginners and experts, focusing on near misses and pitfalls during LH and proposing techniques and principles with which to avoid them. These techniques and principles have guided us to avoid critical pitfalls and near misses during LH and have decreased the intraoperative complication rates at our institution. The magnified views unique to laparoscopic surgery are recognized as a potential advantage over open surgery.9,10 The laparoscopic up-view from the caudal side provides a better operative view behind the liver or around the IVC than does open hepatectomy. However, any surgeon who performs LH must remember that the magnified laparoscopic view itself may ironically mislead surgeons, resulting in critical misjudgments or errors because of the lack of a complete hepatic overview, as demonstrated in Supplementary Videos 2 and 3. In fact, massive bleeding associated with vessel injury or surgical clip slippage (6.1%) occurred due in part to the lack of a hepatic overview. The laparoscopic view from the caudal side of the liver facilitates parenchymal transection during LH. However, it potentially causes injury to the MHV when surgeons lack the anatomic understanding unique to the LH, specifically that the peripheral branch of the MHV is located in close proximity to the hilar plate, as representatively demonstrated in Supplementary Videos 5 and 6. In addition to an understanding of the laparoscopic view and anatomic aspects unique to LH, a systematic technique of intraoperative ultrasonography is helpful for surgeons to avoid
ARTICLE IN PRESS 6 Kawaguchi et al
injury to the hepatic vessels.24 The technologic innovations, such as three-dimensional video systems,25 laparoscopic intraoperative ultrasonography with contrast agents,26 real-time tissue elastography,12 and indocyanine green-fluorescence imaging technique,27 have helped surgeons identify the anatomic structure of the liver. We believe that the techniques and principles demonstrated in the present study are also helpful for surgeons who perform LH. They have developed over a single surgeon’s experiences, however, and therefore need to be addressed by other groups. An increasing number of reports on potential near misses and their solutions are essential to further improve the safety of LH, not to mention a prospective and multicenter approach to minimize intraoperative complications. In conclusion, we have demonstrated the operative techniques and guiding principles with which to address near misses and pitfalls of LH, which are due in large part to the disadvantage of the laparoscopic magnified view and the lack of understanding of the anatomic aspects unique to LH. These techniques and principles are expected to help surgeons to avoid intraoperative complications and ensure the safety of LH. The authors thank Takeo Nomi for coordinating the patients’ follow-up and maintaining the prospective database that formed the basis of this study. SUPPLEMENTARY DATA Supplementary data related to this article can be found online at http://dx.doi.org/10.1016/j.surg.2016.07.023.
REFERENCES 1. Vibert E, Perniceni T, Levard H, Denet C, Shahri NK, Gayet B. Laparoscopic liver resection. Br J Surg 2006;93:67-72. 2. Otsuka Y, Tsuchiya M, Maeda T, Katagiri T, Isii J, Tamura A, et al. Laparoscopic hepatectomy for liver tumors: proposals for standardization. J Hepatobiliary Pancreat Surg 2009;16:720-5. 3. Nitta H, Sasaki A, Fujita T, Itabashi H, Hoshikawa K, Takahara T, et al. Laparoscopy-assisted major liver resections employing a hanging technique: the original procedure. Ann Surg 2010;251:450-3. 4. Nguyen KT, Marsh JW, Tsung A, Steel JJ, Gamblin TC, Geller DA. Comparative benefits of laparoscopic vs open hepatic resection: a critical appraisal. Arch Surg 2011;146:348-56. 5. Cannon RM, Brock GN, Marvin MR, Buell JF. Laparoscopic liver resection: an examination of our first 300 patients. J Am Coll Surg 2011;213:501-7. 6. Hwang DW, Han HS, Yoon YS, Cho JY, Kwon Y, Kim JH, et al. Laparoscopic major liver resection in Korea: a multicenter study. J Hepatobiliary Pancreat Sci 2013;20:125-30. 7. Croome KP, Yamashita MH. Laparoscopic vs open hepatic resection for benign and malignant tumors: An updated meta-analysis. Arch Surg 2010;145:1109-18.
Surgery j 2016
8. Nguyen KT, Gamblin TC, Geller DA. World review of laparoscopic liver resection-2,804 patients. Ann Surg 2009;250:831-41. 9. Hoznek A, Salomon L, Olsson LE, Antiphon P, Saint F, Cicco A, et al. Laparoscopic radical prostatectomy. The Creteil experience. Eur Urol 2001;40:38-45. 10. Asoglu O, Matlim T, Karanlik H, Atar M, Muslumanoglu M, Kapran Y, et al. Impact of laparoscopic surgery on bladder and sexual function after total mesorectal excision for rectal cancer. Surg Endosc 2009;23:296-303. 11. Eiriksson K, Fors D, Rubertsson S, Arvidsson D. High intraabdominal pressure during experimental laparoscopic liver resection reduces bleeding but increases the risk of gas embolism. Br J Surg 2011;98:845-52. 12. Kawaguchi Y, Tanaka N, Nagai M, Nomura Y, Fuks D, Gayet B, et al. Usefulness of intraoperative real-time tissue elastography during laparoscopic hepatectomy. J Am Coll Surg 2015;221:e103-11. 13. Ishizawa T, Gumbs AA, Kokudo N, Gayet B. Laparoscopic segmentectomy of the liver: from segment I to VIII. Ann Surg 2012;256:959-64. 14. Gumbs AA, Gayet B. Adopting Gayet’s techniques of totally laparoscopic liver surgery in the United States. Liver Cancer 2013;2:5-15. 15. Pringle JH. V. Notes on the arrest of hepatic hemorrhage due to trauma. Ann Surg 1908;48:541-9. 16. Couinaud C. Surgical anatomy of the liver revisited. Paris: C. Couinaud; 1989. 17. Mikami S, Hamano T, Fujii N, Nagasawa Y, Isaka Y, Moriyama T, et al. Serum osteoprotegerin as a screening tool for coronary artery calcification score in diabetic predialysis patients. Hypertens Res 2008;31:1163-70. 18. Kanda Y. Investigation of the freely available easy-to-use software ‘EZR’ for medical statistics. Bone Marrow Transplant 2013;48:452-8. 19. Eguchi S, Kanematsu T, Arii S, Okazaki M, Okita K, Omata M, et al. Comparison of the outcomes between an anatomical subsegmentectomy and a non-anatomical minor hepatectomy for single hepatocellular carcinomas based on a Japanese nationwide survey. Surgery 2008;143:469-75. 20. Hasegawa K, Kokudo N, Imamura H, Matsuyama Y, Aoki T, Minagawa M, et al. Prognostic impact of anatomic resection for hepatocellular carcinoma. Ann Surg 2005;242:252-9. 21. Clavien PA, Barkun J, de Oliveira ML, Vauthey JN, Dindo D, Schulick RD, et al. The Clavien-Dindo classification of surgical complications: five-year experience. Ann Surg 2009;250:187-96. 22. Cai X, Li Z, Zhang Y, Yu H, Liang X, Jin R, et al. Laparoscopic liver resection and the learning curve: a 14-year, single-center experience. Surg Endosc 2014;28:1334-41. 23. Vigano L, Laurent A, Tayar C, Tomatis M, Ponti A, Cherqui D. The learning curve in laparoscopic liver resection: improved feasibility and reproducibility. Ann Surg 2009;250:772-82. 24. Araki K, Conrad C, Ogiso S, Kuwano H, Gayet B. Intraoperative ultrasonography of laparoscopic hepatectomy: key technique for safe liver transection. J Am Coll Surg 2014;218:e37-41. 25. Storz P, Buess GF, Kunert W, Kirschniak A. 3D HD versus 2D HD: surgical task efficiency in standardised phantom tasks. Surg Endosc 2012;26:1454-60. 26. Kawaguchi Y, Tanaka N, Kokudo N. Surgical value of contrast-enhanced ultrasonography in laparoscopic hepatectomy using energy devices. J Hepatobiliary Pancreat Sci 2014;21:78-9. 27. Kawaguchi Y, Velayutham V, Fuks D, Christidis C, Kokudo N, Gayet B. Usefulness of indocyanine green-fluorescence imaging for visualization of the bile duct during laparoscopic liver resection. J Am Coll Surg 2015;221:e113-7.