Protective Effect of Minimally Invasive Approach on Postoperative Peak Transaminase Following Liver Resection: A Single-Center Propensity Score-Based Analysis
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Design
2.2. Variables
2.3. Technical Approach
2.3.1. Open Liver Resections (OLR)
2.3.2. Minimally Invasive Liver Surgery (MILS)
2.4. Statistical Analysis
3. Results
3.1. Patient’s Characteristics of the Entire Population
3.2. Patient’s Characteristics after the Stabilized Inverse Probability Treatment Weighting (SIPTW) Process
3.3. ALT Serum Levels on POD 1, 3 and 5
3.4. Postoperative Peak Transaminase (PPT)
3.5. Postoperative Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- LiverGroup.org Collaborative. Outcomes of elective liver surgery worldwide: A global, prospective, multicenter, cross-sectional study. Int. J. Surg. 2023, 109, 3954–3966. [Google Scholar] [CrossRef] [PubMed]
- Sijberden, J.P.; Zimmitti, G.; Cipriani, F.; Furumaya, A.; Lanari, J.; Suhool, A.; Osei-Bordom, D.; Aghayan, D.; Jovine, E.; Ruzzenente, A.; et al. Trends in the characteristics and perioperative outcomes of patients undergoing laparoscopic and open resections for benign liver lesions: An international multicenter retrospective cohort study of 845 patients. HPB 2024, 26, 188–202. [Google Scholar] [CrossRef] [PubMed]
- Belghiti, J.; Noun, R.; Zante, E.; Ballet, T.; Sauvanet, A. Portal triad clamping or hepatic vascular exclusion for major liver resection: A controlled study. Ann. Surg. 1996, 224, 155–161. [Google Scholar] [CrossRef] [PubMed]
- Imamura, H.; Kokudo, N.; Sugawara, Y.; Sano, K.; Kaneko, J.; Takayama, T.; Makuuchi, M. Pringle’s maneuver and selective inflow occlusion in living donor liver hepatectomy. Liver Transplant. 2004, 10, 771–778. [Google Scholar] [CrossRef] [PubMed]
- Giuliante, F.; Ardito, F.; Vellone, M.; Ranucci, G.; Federico, B.; Giovannini, I.; Nuzzo, G. Role of the surgeon as a variable in long-term survival after liver resection for colorectal metastases. J. Surg. Oncol. 2009, 100, 538–545. [Google Scholar] [CrossRef]
- Torzilli, G.; Procopio, F.; Donadon, M.; Del Fabbro, D.; Cimino, M.; Montorsi, M. Safety of intermittent Pringle maneuver cumulative time exceeding 120 minutes in liver resection: A further step in favor of the “radical but conservative” policy. Ann. Surg. 2012, 255, 270–280. [Google Scholar] [CrossRef]
- Nuzzo, G.; Giuliante, F.; Vellone, M.; De Cosmo, G.; Ardito, F.; Murazio, M.; D’Acapito, F.; Giovannini, I. Pedicle clamping with ischemic preconditioning in liver resection. Liver Transplant. 2004, 10, S53–S57. [Google Scholar] [CrossRef]
- Guo, T.; Xiao, Y.; Liu, Z.; Liu, Q. The impact of intraoperative vascular occlusion during liver surgery on postoperative peak ALT levels: A systematic review and meta-analysis. Int. J. Surg. 2016, 27, 99–104. [Google Scholar] [CrossRef] [PubMed]
- Wei, X.; Zheng, W.; Yang, Z.; Liu, H.; Tang, T.; Li, X.; Liu, X. Effect of the intermittent Pringle maneuver on liver damage after hepatectomy: A retrospective cohort study. World J. Surg. Oncol. 2019, 17, 142. [Google Scholar] [CrossRef]
- Boleslawski, E.; Vibert, E.; Pruvot, F.R.; Le Treut, Y.P.; Scatton, O.; Laurent, C.; Mabrut, J.Y.; Régimbeau, J.M.; Adham, M.; Cosse, C.; et al. Relevance of postoperative peak transaminase after elective hepatectomy. Ann. Surg. 2014, 260, 815–820, discussion 820–821. [Google Scholar] [CrossRef]
- Mpabanzi, L.; van Mierlo, K.M.; Malagó, M.; Dejong, C.H.; Lytras, D.; Olde Damink, S.W. Surrogate endpoints in liver surgery related trials: A systematic review of the literature. HPB 2013, 15, 327–336. [Google Scholar] [CrossRef] [PubMed]
- Giovannini, I.; Chiarla, C.; Giuliante, F.; Vellone, M.; Ardito, F.; Sarno, G.; Nuzzo, G. Analysis of the components of hypertransaminasemia after liver resection. Clin. Chem. Lab. Med. 2007, 45, 357–360. [Google Scholar] [CrossRef] [PubMed]
- Ciria, R.; Cherqui, D.; Geller, D.A.; Briceno, J.; Wakabayashi, G. Comparative Short-term Benefits of Laparoscopic Liver Resection: 9000 Cases and Climbing. Ann. Surg. 2016, 263, 761–777. [Google Scholar] [CrossRef] [PubMed]
- Ciria, R.; Berardi, G.; Alconchel, F.; Briceño, J.; Choi, G.H.; Wu, Y.M.; Sugioka, A.; Troisi, R.I.; Salloum, C.; Soubrane, O.; et al. The impact of robotics in liver surgery: A worldwide systematic review and short-term outcomes meta-analysis on 2728 cases. J. Hepatobiliary Pancreat. Sci. 2022, 29, 181–197. [Google Scholar] [CrossRef] [PubMed]
- Abu Hilal, M.; Aldrighetti, L.; Dagher, I.; Edwin, B.; Troisi, R.I.; Alikhanov, R.; Aroori, S.; Belli, G.; Besselink, M.; Briceno, J.; et al. The Southampton Consensus Guidelines for Laparoscopic Liver Surgery: From Indication to Implementation. Ann. Surg. 2018, 268, 11–18. [Google Scholar] [CrossRef] [PubMed]
- Strasberg, S.M.; Belghiti, J.; Clavien, P.A.; Terminology Committee of the IHPBA. Terminology of liver anatomy and resections. HPB Surg. 2000, 2, 333–339. [Google Scholar] [CrossRef]
- Giuliante, F.; Nuzzo, G.; Ardito, F.; Vellone, M.; De Cosmo, G.; Giovannini, I. Extraparenchymal Control of Hepatic Veins During Mesohepatectomy. J. Am. Coll. Surg. 2008, 206, 496–502. [Google Scholar] [CrossRef] [PubMed]
- Giuliante, F.; Ardito, F. Minimally invasive liver surgery in a hepato-biliary unit: Learning curve and indications. Updates Surg. 2015, 67, 201–206. [Google Scholar] [CrossRef] [PubMed]
- Dindo, D.; Demartines, N.; Clavien, P.A. Classification of surgical complications: A new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann. Surg. 2004, 240, 205–213. [Google Scholar] [CrossRef]
- Doi, S.; Yasuda, S.; Hokuto, D.; Kamitani, N.; Matsuo, Y.; Sakata, T.; Nishiwada, S.; Nagai, M.; Nakamura, K.; Terai, T.; et al. Impact of the Prolonged Intermittent Pringle Maneuver on Post-Hepatectomy Liver Failure: Comparison of Open and Laparoscopic Approaches. World J. Surg. 2023, 47, 3328–3337. [Google Scholar] [CrossRef]
- Mownah, O.A.; Aroori, S. The Pringle maneuver in the modern era: A review of techniques for hepatic inflow occlusion in minimally invasive liver resection. Ann. Hepatobiliary Pancreat. Surg. 2023, 27, 131–140. [Google Scholar] [CrossRef] [PubMed]
- Wang, F.; Lu, J.; Yang, T.; Ren, Y.; Ratti, F.; Marques, H.P.; Silva, S.; Soubrane, O.; Lam, V.; Poultsides, G.A.; et al. Perioperative Changes in Serum Transaminase Levels: Impact on Postoperative Morbidity Following Liver Resection of Hepatocellular Carcinoma. Ann. Surg. 2024; online ahead of print. [Google Scholar] [CrossRef] [PubMed]
- van de Poll, M.C.; Derikx, J.P.; Buurman, W.A.; Peters, W.H.; Roelofs, H.M.; Wigmore, S.J.; Dejong, C.H. Liver manipulation causes hepatocyte injury and precedes systemic inflammation in patients undergoing liver resection. World J. Surg. 2007, 31, 2033–2038. [Google Scholar] [CrossRef] [PubMed]
- van den Broek, M.A.; Shiri-Sverdlov, R.; Schreurs, J.J.; Bloemen, J.G.; Bieghs, V.; Rensen, S.S.; Dejong, C.H.; Olde Damink, S.W. Liver manipulation during liver surgery in humans is associated with hepatocellular damage and hepatic inflammation. Liver Int. 2013, 33, 633–641. [Google Scholar] [CrossRef] [PubMed]
- Liu, C.L.; Fan, S.T.; Cheung, S.T.; Lo, C.M.; Ng, I.O.; Wong, J. Anterior approach versus conventional approach right hepatic resection for large hepatocellular carcinoma: A prospective randomized controlled study. Ann. Surg. 2006, 244, 194–203. [Google Scholar] [CrossRef] [PubMed]
- Lesurtel, M.; Selzner, M.; Petrowsky, H.; McCormack, L.; Clavien, P.A. How should transection of the liver be performed?: A prospective randomized study in 100 consecutive patients: Comparing four different transection strategies. Ann. Surg. 2005, 242, 814–822, discussion 822–823. [Google Scholar] [CrossRef] [PubMed]
- Pamecha, V.; Gurusamy, K.S.; Sharma, D.; Davidson, B.R. Techniques for liver parenchymal transection: A meta-analysis of randomized controlled trials. HPB 2009, 11, 275–281. [Google Scholar] [CrossRef] [PubMed]
- Rahbari, N.N.; Elbers, H.; Koch, M.; Vogler, P.; Striebel, F.; Bruckner, T.; Mehrabi, A.; Schemmer, P.; Büchler, M.W.; Weitz, J. Randomized clinical trial of stapler versus clamp-crushing transection in elective liver resection. Br. J. Surg. 2014, 101, 200–207. [Google Scholar] [CrossRef]
- Fuchs, J.; Ruping, F.; Murtha-Lemekhova, A.; Kessler, M.; Günther, P.; Mehrabi, A.; Hoffmann, K. Comparison of transection techniques in pediatric major hepatectomy: A matched pair analysis. HPB 2023, 25, 593–601. [Google Scholar] [CrossRef]
- Accardo, C.; Gruttadauria, S.; Decarlis, L.; Agnes, S.; Schmeding, M.; Avolio, A.W.; Buscemi, V.; Ardito, F.; Kienlein, S.; Mbuvi, P.M.; et al. The CUSA Clarity Soft Tissue Removal Study: Clinical Performance Investigation of the CUSA Clarity Ultrasonic Surgical Aspirator System for Soft Tissue Removal During Liver Surgery. J. Laparoendosc. Adv. Surg. Tech. A 2024, 34, 99–105. [Google Scholar] [CrossRef]
- Olthof, P.B.; Huiskens, J.; Schulte, N.R.; Wicherts, D.A.; Besselink, M.G.; Busch, O.R.; Heger, M.; van Gulik, T.M. Postoperative peak transaminases correlate with morbidity and mortality after liver resection. HPB 2016, 18, 915–921. [Google Scholar] [CrossRef] [PubMed]
OLR (348) | MILS (258) | p-Value | |
---|---|---|---|
Male, no. (%) | 204 (58.6) | 155 (60.1) | 0.78 |
Female, no. (%) | 144 (41.4) | 103 (39.9) | |
Age, median (IQR), yr | 64 (56–70) | 63 (53–71) | 0.10 |
Benign disease, no. (%) | 32 (9.2) | 68 (26.4) | <0.001 |
Malignant disease, no. (%) | 316 (90.8) | 190 (73.6) | |
Metastases | 254 (73.0) | 117 (45.3) | <0.001 |
HCC | 37 (10.6) | 63 (24.4) | <0.001 |
Cholangiocarcinoma | 25 (7.2) | 10 (3.9) | 0.08 |
Major resection, no. (%) | 107 (30.7) | 24 (9.3) | <0.001 |
Multiple resections (no. ≥ 3), no. (%) | 82 (23.6) | 8 (3.1) | <0.001 |
Use of pedicle clamping, no. (%) | 294 (84.5) | 196 (76.0) | 0.008 |
Clamping time, median (IQR), minutes | 67 (45–97) | 60 (31–96) | 0.03 |
Clamping time ≥ 120 min, no. (%) | 45 (12.9) | 25 (9.7) | 0.21 |
Intraoperative blood transfusions, no. (%) | 26 (7.5) | 1 (0.4) | <0.001 |
Duration of surgery, median (IQR), minutes | 390 (305–502) | 300 (220–400) | <0.001 |
OLR (159) | MILS (292) | p-Value | |
---|---|---|---|
Male, no. (%) | 93 (58.5%) | 165 (56.5%) | 0.69 |
Female, no. (%) | 66 (41.5%) | 127 (43.5%) | |
Age, median (IQR), yr | 64 (55–70) | 63 (51–72) | 0.18 |
Benign disease, no. (%) | 28 (17.6%) | 64 (21.9%) | 0.33 |
Malignant disease, no. (%) | 130 (82.0%) | 227 (77.7%) | |
Metastases | 97 (61.0%) | 149 (51.0%) | 0.06 |
HCC | 25 (15.7%) | 59 (20.2%) | 0.31 |
Cholangiocarcinoma | 9 (5.7%) | 20 (6.9%) | 0.69 |
Major resection, no. (%) | 34 (21.4%) | 49 (16.8%) | 0.25 |
Multiple resections (no. ≥ 3), no. (%) | 23 (14.6%) | 29 (9.9%) | 0.17 |
Use of pedicle clamping, no. (%) | 132 (83.0%) | 231 (79.1%) | 0.38 |
Clamping time, median (IQR), minutes | 58 (20–89) | 47 (15–88) | 0.39 |
Clamping time ≥ 120 min, no. (%) | 19 (11.9) | 41 (14.0) | 0.57 |
Intraoperative blood transfusions, no. (%) | 7 (4.4%) | 14 (4.8%) | 1.00 |
Duration of surgery, median (IQR), minutes | 346 (287–477) | 340 (244–480) | 0.27 |
(a) | |||
---|---|---|---|
OLR (348) | MILS (258) | p-Value | |
ALT levels, median (IQR) | |||
POD 1 | 334 (207–570) | 164 (94–324) | <0.0001 |
POD 3 | 196 (118–326) | 109 (58–193) | <0.0001 |
POD 5 | 109 (64–55) | 53 (34–01) | <0.0001 |
(b) | |||
OLR (159) | MILS (292) | p-Value | |
ALT levels, median (IQR) | |||
POD 1 | 301 (192–566) | 187 (104–349) | 0.002 |
POD 3 | 180 (114–308) | 121 (65–213) | <0.0001 |
POD 5 | 104 (64–53) | 60 (37–15) | <0.0001 |
(a) | |||
---|---|---|---|
OLR (n = 45) | MILS (n = 25) | p-Value | |
ALT levels, median (IQR) | |||
POD 1 | 586 (411–952) | 346 (291–584) | 0.004 |
POD 3 | 309 (218–515) | 225 (162–357) | 0.047 |
POD 5 | 154 (107–239) | 121 (74–178) | 0.08 |
(b) | |||
OLR (n = 19) | MILS (n = 41) | p-Value | |
POD 1 | 730 (436–1302) | 611 (324–1251) | 0.15 |
POD 3 | 373 (246–749) | 351 (197–429) | 0.07 |
POD 5 | 196 (132–278) | 176 (114–233) | 0.02 |
Beta | SE | Wald | OR | Lower | Upper | p-Value | |
---|---|---|---|---|---|---|---|
MILS | −0.920 | 0.244 | 14.223 | 0.399 | 0.247 | 0.643 | <0.001 |
Duration of pedicle clamping | 0.022 | 0.003 | 63.078 | 1.022 | 1.016 | 1.027 | <0.001 |
Age | −0.025 | 0.009 | 6.693 | 0.976 | 0.958 | 0.994 | 0.010 |
Multiple resections (no. ≥ 3) | 1.063 | 0.385 | 7.623 | 2.894 | 1.361 | 6.152 | 0.006 |
Beta | SE | Wald | OR | Lower | Upper | p-Value | |
---|---|---|---|---|---|---|---|
Clavien–Dindo ≥ 3 | |||||||
MILS | −1.72 | 0.57 | 9.23 | 0.18 | 0.06 | 0.54 | 0.002 |
High PPT-ALT on POD 1 | 0.99 | 0.51 | 3.84 | 2.69 | 1.01 | 7.24 | 0.049 |
Re-intervention | |||||||
High PPT-ALT on POD 1 | 2.88 | 0.98 | 8.66 | 17.81 | 2.62 | 121.31 | 0.003 |
Benign disease | 2.23 | 0.87 | 6.60 | 9.32 | 1.70 | 51.10 | 0.01 |
Cholangiocellular cancer | 2.62 | 1.18 | 4.98 | 13.77 | 1.38 | 137.89 | 0.03 |
Age, yr | 0.07 | 0.03 | 4.59 | 1.08 | 1.01 | 1.15 | 0.03 |
Prolonged postoperative stay (>10 days) | |||||||
MILS | −2.99 | 0.78 | 14.87 | 0.05 | 0.01 | 0.23 | <0.001 |
Duration of surgery | 0.004 | 0.002 | 5.60 | 1.00 | 1.001 | 1.01 | 0.02 |
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Ardito, F.; Ingallinella, S.; Lai, Q.; Razionale, F.; De Sio, D.; Mele, C.; Vani, S.; Vellone, M.; Giuliante, F. Protective Effect of Minimally Invasive Approach on Postoperative Peak Transaminase Following Liver Resection: A Single-Center Propensity Score-Based Analysis. Cancers 2024, 16, 2605. https://doi.org/10.3390/cancers16142605
Ardito F, Ingallinella S, Lai Q, Razionale F, De Sio D, Mele C, Vani S, Vellone M, Giuliante F. Protective Effect of Minimally Invasive Approach on Postoperative Peak Transaminase Following Liver Resection: A Single-Center Propensity Score-Based Analysis. Cancers. 2024; 16(14):2605. https://doi.org/10.3390/cancers16142605
Chicago/Turabian StyleArdito, Francesco, Sara Ingallinella, Quirino Lai, Francesco Razionale, Davide De Sio, Caterina Mele, Simone Vani, Maria Vellone, and Felice Giuliante. 2024. "Protective Effect of Minimally Invasive Approach on Postoperative Peak Transaminase Following Liver Resection: A Single-Center Propensity Score-Based Analysis" Cancers 16, no. 14: 2605. https://doi.org/10.3390/cancers16142605
APA StyleArdito, F., Ingallinella, S., Lai, Q., Razionale, F., De Sio, D., Mele, C., Vani, S., Vellone, M., & Giuliante, F. (2024). Protective Effect of Minimally Invasive Approach on Postoperative Peak Transaminase Following Liver Resection: A Single-Center Propensity Score-Based Analysis. Cancers, 16(14), 2605. https://doi.org/10.3390/cancers16142605