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Laparoscopic liver resection reduces postoperative infection in patients with hepatocellular carcinoma: a propensity score-based analysis

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Abstract

Background

This study is aimed to compare the occurrence of postoperative infections between patients with hepatocellular carcinoma (HCC) undergoing laparoscopic liver resection (LLR) and those undergoing open liver resection (OLR).

Methods

This study included 446 patients who underwent initial curative liver resection for HCC 5 cm or less in size without macroscopic vascular invasion. To adjust for confounding factors between the LLR and OLR groups, propensity score matching and inverse probability weighting (IPW) analysis were performed. The incidence rates of postoperative infection, including incisional surgical site infection (SSI), organ/space SSI, and remote infection (RI), were compared between the two groups.

Results

An imbalance in several confounding variables, including period of surgery, extent of liver resection, difficult location, proximity to a major vessel, tumor size ≥ 3 cm, and multiple tumors, was observed between the two groups in the original cohort. After matching and weighting, the imbalance between the two groups significantly decreased. Compared with OLR, LLR was associated with a lower volume of intraoperative blood loss (140 vs. 350 mL, P < 0.001 in the matched cohort; 120 vs. 320 mL, P < 0.001 in the weighted cohort) and reduced risk of postoperative infection (2.0% vs. 12%, P = 0.015 in the matched cohort; 2.9% vs. 14%, P = 0.005 in the weighted cohort). Of the types of postoperative infections, organ/space SSI and RI were less frequently observed in the LLR group than in the OLR group in the matched cohort (1.0% vs. 6.0%, P = 0.091 for organ/space SSI; 0% vs. 6.0%, P < 0.001 for RI) and in the weighted cohort (1.2% vs. 7.8%, P < 0.001 for organ/space SSI; 0.3% vs. 5.1%, P = 0.009 for RI).

Conclusions

Compared with OLR, LLR for HCC might reduce postoperative infections, including organ/space SSI and RI.

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References

  1. Fortner JG, Kim DK, Maclean BJ, Barrett MK, Iwatsuki S, Turnbull AD et al (1978) Major hepatic resection for neoplasia: personal experience in 108 patients. Ann Surg 188:363–371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Kenjo A, Miyata H, Gotoh M, Kitagawa Y, Shimada M, Baba H et al (2014) Risk stratification of 7732 hepatectomy cases in 2011 from the National clinical database for Japan. J Am Coll Surg 218:412–422

    Article  PubMed  Google Scholar 

  3. Kingham TP, Correa-Gallego C, D’Angelica MI, Gönen M, Dematteo RP, Fong Y et al (2015) Hepatic parenchymal preservation surgery: decreasing morbidity and mortality rates in 4152 resections for malignancy. J Am Coll Surg 220:471–479

    Article  PubMed  Google Scholar 

  4. Gani F, Cerullo M, Amini N, Buettner S, Margonis GA, Sasaki K et al (2017) Frailty as a risk predictor of morbidity and mortality following liver surgery. J Gastrointest Surg 21:822–830

    Article  PubMed  Google Scholar 

  5. Togo S, Tanaka K, Matsuo K, Nagano Y, Ueda M, Morioka D et al (2007) Duration of antimicrobial prophylaxis in patients undergoing hepatectomy: a prospective randomized controlled trial using flomoxef. J Antimicrob Chemother 59:964–970

    Article  CAS  PubMed  Google Scholar 

  6. Hirokawa F, Hayashi M, Miyamoto Y, Asakuma M, Shimizu T, Komeda K et al (2013) Evaluation of postoperative antibiotic prophylaxis after liver resection: a randomized controlled trial. Am J Surg 206:8–15

    Article  PubMed  Google Scholar 

  7. Zhou Y-M, Chen Z-Y, Li X-D, Xu D-H, Su X, Li B (2016) Preoperative antibiotic prophylaxis does not reduce the risk of postoperative infectious complications in patients undergoing elective hepatectomy. Dig Dis Sci 61:1707–1713

    Article  CAS  PubMed  Google Scholar 

  8. Sadamori H, Yagi T, Shinoura S, Umeda Y, Yoshida R, Satoh D et al (2013) Risk factors for organ/space surgical site infection after hepatectomy for hepatocellular carcinoma in 359 recent cases. J Hepatobiliary Pancreat Sci 20:186–196

    Article  PubMed  Google Scholar 

  9. Nanashima A, Arai J, Oyama S, Ishii M, Abo T, Wada H et al (2014) Associated factors with surgical site infections after hepatectomy: predictions and countermeasures by a retrospective cohort study. Int J Surg 12:310–314

    Article  PubMed  Google Scholar 

  10. Tang H, Lu W, Yang Z, Jiang K, Chen Y, Lu S et al (2017) Risk factors and long-term outcome for postoperative intra-abdominal infection after hepatectomy for hepatocellular carcinoma. Medicine (Baltimore) 96:e6795

    Article  Google Scholar 

  11. Takahara T, Wakabayashi G, Beppu T, Aihara A, Hasegawa K, Gotohda N et al (2015) Long-term and perioperative outcomes of laparoscopic versus open liver resection for hepatocellular carcinoma with propensity score matching: a multi-institutional Japanese study. J Hepatobiliary Pancreat Sci 22:721–727

    Article  PubMed  Google Scholar 

  12. Wakabayashi G, Cherqui D, Geller DA, Buell JF, Kaneko H, Han HS et al (2015) Recommendations for laparoscopic liver resection: a report from the second international consensus conference held in Morioka. Ann Surg 261:619–629

    PubMed  Google Scholar 

  13. Ciria R, Cherqui D, Geller DA, Briceno J, Wakabayashi G (2016) Comparative short-term benefits of laparoscopic liver resection: 9000 cases and climbing. Ann Surg 263:761–777

    Article  PubMed  Google Scholar 

  14. Shehta A, Han HS, Yoon YS, Cho JY, Choi Y (2016) Laparoscopic liver resection for hepatocellular carcinoma in cirrhotic patients: 10-year single-center experience. Surg Endosc 30:638–648

    Article  PubMed  Google Scholar 

  15. Martinez-Cecilia D, Cipriani F, Shelat V, Ratti F, Tranchart H, Barkhatov L et al (2017) Laparoscopic versus open liver resection for colorectal metastases in elderly and octogenarian patients: a multicenter propensity score based analysis of short- and long-term outcomes. Ann Surg 265:1192–1200

    Article  PubMed  Google Scholar 

  16. Scuderi V, Barkhatov L, Montalti R, Ratti F, Cipriani F, Pardo F et al (2017) Outcome after laparoscopic and open resections of posterosuperior segments of the liver. Br J Surg 104:751–759

    Article  CAS  PubMed  Google Scholar 

  17. Miyagi S, Nakanishi C, Hara Y, Kamei T, Kawagishi N, Ohuchi N (2015) An evaluation of the safety of pure laparoscopic hepatectomy in patients with liver cirrhosis: investigations including serum albumin and ascites. Surg Laparosc Endosc Percutan Tech 25:209–211

    Article  PubMed  Google Scholar 

  18. López-Ben S, Palacios O, Codina-Barreras A, Albiol MT, Falgueras L, Castro E et al (2014) Pure laparoscopic liver resection reduces surgical site infections and hospital stay. Results of a case-matched control study in 50 patients. Langenbeck’s Archives of Surgery. 399:307–314

    Article  PubMed  Google Scholar 

  19. Matsukuma S, Tokumitsu Y, Nakagami Y, Shindo Y, Matsui H, Nakajima M et al (2021) Laparoscopic resection reduces superficial surgical site infection in liver surgery. Surg Endosc 35:7131–7141

    Article  PubMed  Google Scholar 

  20. Cheung TT, Han H-S, She WH, Chen K-H, Chow PKH, Yoong BK et al (2018) The Asia Pacific consensus statement on laparoscopic liver resection for hepatocellular carcinoma: a report from the 7th Asia-Pacific primary liver cancer expert meeting held in Hong Kong. Liver Cancer 7:28–39

    Article  PubMed  Google Scholar 

  21. Makuuchi M, Kosuge T, Takayama T, Yamazaki S, Kakazu T, Miyagawa S et al (1993) Surgery for small liver cancers. Semin Surg Oncol 9:298–304

    Article  CAS  PubMed  Google Scholar 

  22. Tanaka S, Takemura S, Shinkawa H, Nishioka T, Hamano G, Kinoshita M et al (2015) Outcomes of pure laparoscopic versus open hepatic resection for hepatocellular carcinoma in cirrhotic patients: a case-control study with propensity score matching. Eur Surg Res 55:291–301

    Article  PubMed  Google Scholar 

  23. Kinoshita M, Shinkawa H, Kabata D, Tanaka S, Takemura S, Amano R et al (2021) Impact of advancing age on the status and risk of postoperative infections after liver resection. World J Surg 45:3386–3394

    Article  PubMed  Google Scholar 

  24. Berríos-Torres SI, Umscheid CA, Bratzler DW, Leas B, Stone EC, Kelz RR et al (2017) Centers for disease control and prevention guideline for the prevention of surgical site infection, 2017. JAMA Surg 152:784

    Article  PubMed  Google Scholar 

  25. Chan KM, Lee CF, Wu TJ, Chou HS, Yu MC, Lee WC et al (2012) Adverse outcomes in patients with postoperative ascites after liver resection for hepatocellular carcinoma. World J Surg 36:392–400

    Article  PubMed  Google Scholar 

  26. Koch M, Garden OJ, Padbury R, Rahbari NN, Adam R, Capussotti L et al (2011) Bile leakage after hepatobiliary and pancreatic surgery: a definition and grading of severity by the International Study Group of Liver Surgery. Surgery 149:680–688

    Article  PubMed  Google Scholar 

  27. Dindo D, Demartines N, Clavien PA (2004) Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 240:205–213

    Article  PubMed  PubMed Central  Google Scholar 

  28. Rosenbaum PR, Rubin DB (1984) Reducing bias in observational studies using subclassification on the propensity score. J Am Stat Assoc 79:516–524

    Article  Google Scholar 

  29. Kabata D, Shintani A (2022) Estimating the treatment effect with propensity score when the effect varies by patient characteristics: A case study and simulation. Communications in Statistics: Case Studies, Data Analysis and Applications 1–13

  30. Cho JY, Han H-S, Yoon Y-S, Shin S-H (2008) Experiences of laparoscopic liver resection including lesions in the posterosuperior segments of the liver. Surg Endosc 22:2344–2349

    Article  PubMed  Google Scholar 

  31. Stuart EA (2010) Matching methods for causal inference: a review and a look forward. Stat Sci 25:1–21

    Article  PubMed  PubMed Central  Google Scholar 

  32. Imai K, Ratkovic M (2014) Covariate balancing propensity score. J Royal Stat Soc 76:243–263

    Article  Google Scholar 

  33. Austin PC, Stuart EA (2015) Moving towards best practice when using inverse probability of treatment weighting (IPTW) using the propensity score to estimate causal treatment effects in observational studies. Stat Med 34:3661–3679

    Article  PubMed  PubMed Central  Google Scholar 

  34. Takesue Y, Kusachi S, Mikamo H, Sato J, Watanabe A, Kiyota H et al (2018) Antimicrobial susceptibility of common pathogens isolated from postoperative intra-abdominal infections in Japan. J Infect Chemother 24:330–340

    Article  CAS  PubMed  Google Scholar 

  35. Nishizaki T, Matsumata T, Yanaga K, Shimada M, Higashi H, Sugimachi K (1993) Open and closed suction drainage after hepatic resection. Surg Today 23:871–874

    Article  CAS  PubMed  Google Scholar 

  36. Shirata C, Hasegawa K, Kokudo T, Arita J, Akamatsu N, Kaneko J et al (2018) Surgical site infection after hepatectomy for hepatocellular carcinoma. Dig Surg 35:204–211

    Article  PubMed  Google Scholar 

  37. Jildeh TR, Okoroha KR, Marshall NE, Abdul-Hak A, Zeni F, Moutzouros V (2018) Infection and rerupture after surgical repair of achilles tendons. Orthop J Sports Med 6:232596711877430

    Article  Google Scholar 

  38. Matsuo Y, Nomi T, Hokuto D, Yoshikawa T, Kamitani N, Sho M (2020) Pulmonary complications after laparoscopic liver resection. Surg Endosc 35:1659–1666

    Article  PubMed  Google Scholar 

  39. Fuks D, Cauchy F, Ftériche S, Nomi T, Schwarz L, Dokmak S et al (2016) Laparoscopy decreases pulmonary complications in patients undergoing major liver resection. Ann Surg 263:353–361

    Article  PubMed  Google Scholar 

  40. Alkaaki A, Al-Radi OO, Khoja A, Alnawawi A, Alnawawi A, Maghrabi A et al (2019) Surgical site infection following abdominal surgery: a prospective cohort study. Can J Surg 62:111–117

    Article  PubMed  PubMed Central  Google Scholar 

  41. Caroff DA, Chan C, Kleinman K, Calderwood MS, Wolf R, Wick EC et al (2019) Association of open approach vs laparoscopic approach with risk of surgical site infection after colon surgery. JAMA Netw Open 2:e1913570

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by Health, Labour and Welfare Policy Research Grants from the Ministry of Health, Labour, and Welfare of Japan (Policy Research for Hepatitis Measures [H30-Kansei-Shitei-003]).

Funding

This work was supported by Health, Labour and Welfare Policy Research Grants from the Ministry of Health, Labour, and Welfare of Japan (Policy Research for Hepatitis Measures [H30-Kansei-Shitei-003]).

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Correspondence to Hiroji Shinkawa.

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Daisuke Shirai, Hiroji Shinkawa, Daijiro Kabata, Shigekazu Takemura, Shogo Tanaka, Ryosuke Amano, Kenjiro Kimura, Go Ohira, Kohei Nishio, Jun Tauchi, Masahiko Kinoshita, and Shoji Kubo have no conflicts of interest or financial ties to disclose.

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Shirai, D., Shinkawa, H., Kabata, D. et al. Laparoscopic liver resection reduces postoperative infection in patients with hepatocellular carcinoma: a propensity score-based analysis. Surg Endosc 36, 9194–9203 (2022). https://doi.org/10.1007/s00464-022-09403-7

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  • DOI: https://doi.org/10.1007/s00464-022-09403-7

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