Abstract
Purpose
The study aimed to compare, using propensity score matching (PSM) analyses, the short- and long-term results of laparoscopic colectomy (LC) versus open colectomy (OC) in a bicentric cohort of patients with T4 colon cancer.
Methods
This is a retrospective PSM analysis of consecutive patients undergoing elective LC or OC for pT4 colon cancer (TNM stage II/III) between 2005 and 2014.
Results
Overall, 237 patients were selected. After PSM, 106 LC-and 106 OC-matched patients were compared. LC was associated with longer operative time and lower blood loss than OC (220 vs. 190 min, p < 0.0001; 116 vs. 150 mL, p = 0.002, respectively). LC patients showed a faster recovery, which translated into a shorter hospital stay compared to OC (10.5 vs. 15.3 days, p < 0.0001). Conversion was required in 13 (12.2 %) LC patients. No group difference was observed for 30- and 90-day mortality. R0 resection was achieved in the majority of LC and OC patients (93.9 %). The 1-, 3-, and 5-year overall survival was 99, 76.8, and 58.6 %, respectively, for the LC group and 98, 70.1, and 59.9 %, respectively, for the OC group (p = 0.864). The 1-, 3-, and 5-year disease-free survival was 86.3, 66, 57.6 %, respectively, for the LC group and 79.1, 55.1, and 50.2 % for the OC group (p = 0.261).
Conclusion
With an acceptable conversion rate, laparoscopy can achieve complete oncologic resections of T4 colon cancer similar to open surgery and can be considered a safe and feasible alternative approach that confers the advantage of a faster recovery.
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References
Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D, Bray F (2013) Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 49(6):1374–1403. doi:10.1016/j.ejca.2012.12.027
Snaebjornsson P, Coupe VM, Jonasson L, Meijer GA, van Grieken NC, Jonasson JG (2014) pT4 stage II and III colon cancers carry the worst prognosis in a nationwide survival analysis. Shepherd's local peritoneal involvement revisited. Int J Cancer 135(2):467–478. doi:10.1002/ijc.28676
Gill S, Loprinzi CL, Sargent DJ, Thome SD, Alberts SR, Haller DG, Benedetti J, Francini G, Shepherd LE, Francois Seitz J, Labianca R, Chen W, Cha SS, Heldebrant MP, Goldberg RM (2004) Pooled analysis of fluorouracil-based adjuvant therapy for stage II and III colon cancer: who benefits and by how much? J Clin Oncol 22(10):1797–1806. doi:10.1200/JCO.2004.09.059
Merkel S, Wein A, Gunther K, Papadopoulos T, Hohenberger W, Hermanek P (2001) High-risk groups of patients with stage II colon carcinoma. Cancer 92(6):1435–1443
Edge SB, Compton CC (2010) The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol 17(6):1471–1474. doi:10.1245/s10434-010-0985-4
Lee YC, Lee YL, Chuang JP, Lee JC (2013) Differences in survival between colon and rectal cancer from SEER data. PLoS One 8(11):e78709. doi:10.1371/journal.pone.0078709
Siegel RL, Miller KD, Jemal A (2015) Cancer statistics, 2015. CA Cancer J Clin 65(1):5–29. doi:10.3322/caac.21254
Valentini V, Coco C, Rizzo G, Manno A, Crucitti A, Mattana C, Ratto C, Verbo A, Vecchio FM, Barbaro B, Gambacorta MA, Montoro C, Barba MC, Sofo L, Papa V, Menghi R, D'Ugo DM, Doglietto G (2009) Outcomes of clinical T4M0 extra-peritoneal rectal cancer treated with preoperative radiochemotherapy and surgery: a prospective evaluation of a single institutional experience. Surgery 145(5):486–494. doi:10.1016/j.surg.2009.01.007
Colon Cancer Laparoscopic or Open Resection Study G, Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, Haglind E, Pahlman L, Cuesta MA, Msika S, Morino M, Lacy A, Bonjer HJ (2009) Survival after laparoscopic surgery versus open surgery for colon cancer: long-term outcome of a randomised clinical trial. Lancet Oncol 10(1):44–52. doi:10.1016/S1470-2045(08)70310-3
Bretagnol F, Dedieu A, Zappa M, Guedj N, Ferron M, Panis Y (2011) T4 colorectal cancer: is laparoscopic resection contraindicated? Color Dis 13(2):138–143. doi:10.1111/j.1463-1318.2010.02380.x
Nakafusa Y, Tanaka T, Tanaka M, Kitajima Y, Sato S, Miyazaki K (2004) Comparison of multivisceral resection and standard operation for locally advanced colorectal cancer: analysis of prognostic factors for short-term and long-term outcome. Dis Colon rectum 47(12):2055–2063. doi:10.1007/s10350-004-0716-7
Huh JW, Kim HR (2012) The feasibility of laparoscopic resection compared to open surgery in clinically suspected T4 colorectal cancer. J Laparoendosc Adv Surg Tech A 22(5):463–467. doi:10.1089/lap.2011.0425
Kim KY, Hwang DW, Park YK, Lee HS (2012) A single surgeon's experience with 54 consecutive cases of multivisceral resection for locally advanced primary colorectal cancer: can the laparoscopic approach be performed safely? Surg Endosc 26(2):493–500. doi:10.1007/s00464-011-1907-7
Ng DC, Co CS, Cheung HY, Chung CC, Li MK (2011) The outcome of laparoscopic colorectal resection in T4 cancer. Color Dis 13(10):e349–e352. doi:10.1111/j.1463-1318.2011.02698.x
Shukla PJ, Trencheva K, Merchant C, Maggiori L, Michelassi F, Sonoda T, Lee SW, Milsom JW (2015) Laparoscopic resection of t4 colon cancers: is it feasible? Dis Colon rectum 58(1):25–31. doi:10.1097/DCR.0000000000000220
Vignali A, Ghirardelli L, Di Palo S, Orsenigo E, Staudacher C (2013) Laparoscopic treatment of advanced colonic cancer: a case-matched control with open surgery. Color Dis 15(8):944–948. doi:10.1111/codi.12170
Kim IY, Kim BR, Kim YW (2015) The short-term and oncologic outcomes of laparoscopic versus open surgery for T4 colon cancer. Surg Endosc. doi:10.1007/s00464-015-4364-x
Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AM, Heath RM, Brown JM, group MCt (2005) Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet 365(9472):1718–1726. doi:10.1016/S0140-6736(05)66545-2
Jayne DG, Thorpe HC, Copeland J, Quirke P, Brown JM, Guillou PJ (2010) Five-year follow-up of the Medical Research Council CLASICC trial of laparoscopically assisted versus open surgery for colorectal cancer. Br J Surg 97(11):1638–1645. doi:10.1002/bjs.7160
Lacy AM, Garcia-Valdecasas JC, Delgado S, Castells A, Taura P, Pique JM, Visa J (2002) Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet 359(9325):2224–2229. doi:10.1016/S0140-6736(02)09290-5
Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, Haglind E, Pahlman L, Cuesta MA, Msika S, Morino M, Lacy AM, Group COcLoORS (2005) Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol 6(7):477–484. doi:10.1016/S1470-2045(05)70221-7
Clinical Outcomes of Surgical Therapy Study G (2004) A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med 350(20):2050–2059. doi:10.1056/NEJMoa032651
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(2):205–213
Austin PC (2011) An introduction to propensity score methods for reducing the effects of confounding in observational studies. Multivariate Behav Res 46(3):399–424. doi:10.1080/00273171.2011.568786
Heinze G, Juni P (2011) An overview of the objectives of and the approaches to propensity score analyses. Eur Heart J 32(14):1704–1708. doi:10.1093/eurheartj/ehr031
Austin PC (2009) The relative ability of different propensity score methods to balance measured covariates between treated and untreated subjects in observational studies. Med Decis Mak 29(6):661–677. doi:10.1177/0272989X09341755
Austin PC (2009) Balance diagnostics for comparing the distribution of baseline covariates between treatment groups in propensity-score matched samples. Stat Med 28(25):3083–3107. doi:10.1002/sim.3697
Thoemmes F (2011) An SPSS R menu for propensity score matching. http://arxiv.org/abs/1201.6385
Lonjon G, Boutron I, Trinquart L, Ahmad N, Aim F, Nizard R, Ravaud P (2014) Comparison of treatment effect estimates from prospective nonrandomized studies with propensity score analysis and randomized controlled trials of surgical procedures. Ann Surg 259(1):18–25. doi:10.1097/SLA.0000000000000256
Clavien PA, Puhan MA (2014) Biased reporting in surgery. Br J Surg 101(6):591–592. doi:10.1002/bjs.9499
Hemmila MR, Birkmeyer NJ, Arbabi S, Osborne NH, Wahl WL, Dimick JB (2010) Introduction to propensity scores: a case study on the comparative effectiveness of laparoscopic vs open appendectomy. Arch Surg 145(10):939–945. doi:10.1001/archsurg.2010.193
Ishihara S, Watanabe T, Nagawa H (2008) Intraoperative colonoscopy for stapled anastomosis in colorectal surgery. Surg Today 38(11):1063–1065. doi:10.1007/s00595-007-3740-0
Nelson HD, Cooney TG, Kroenke K, Friedman RH (2000) Contributions of general internal medicine teaching units: a national survey. J Gen Intern Med 15(5):277–283
Winawer S, Fletcher R, Rex D, Bond J, Burt R, Ferrucci J, Ganiats T, Levin T, Woolf S, Johnson D, Kirk L, Litin S, Simmang C, Gastrointestinal Consortium P (2003) Colorectal cancer screening and surveillance: clinical guidelines and rationale—update based on new evidence. Gastroenterology 124(2):544–560. doi:10.1053/gast.2003.50044
Elnahas A, Sunil S, Jackson TD, Okrainec A, Quereshy FA (2015) Laparoscopic versus open surgery for T4 colon cancer: evaluation of margin status. Surg Endosc. doi:10.1007/s00464-015-4360-1
Thorpe H, Jayne DG, Guillou PJ, Quirke P, Copeland J, Brown JM, Medical Research Council Conventional versus Laparoscopic-Assisted Surgery In Colorectal Cancer Trial G (2008) Patient factors influencing conversion from laparoscopically assisted to open surgery for colorectal cancer. Br J Surg 95(2):199–205. doi:10.1002/bjs.5907
Li J, Guo H, Guan XD, Cai CN, Yang LK, Li YC, Zhu YH, Li PP, Liu XL, Yang DJ (2015) The impact of laparoscopic converted to open colectomy on short-term and oncologic outcomes for colon cancer. J Gastrointest Surg 19(2):335–343. doi:10.1007/s11605-014-2685-z
Lehnert T, Methner M, Pollok A, Schaible A, Hinz U, Herfarth C (2002) Multivisceral resection for locally advanced primary colon and rectal cancer: an analysis of prognostic factors in 201 patients. Ann Surg 235(2):217–225
Kiran RP, El-Gazzaz GH, Vogel JD, Remzi FH (2010) Laparoscopic approach significantly reduces surgical site infections after colorectal surgery: data from national surgical quality improvement program. J Am Coll Surg 211(2):232–238. doi:10.1016/j.jamcollsurg.2010.03.028
Network NCC (2012) NCCN clinical practice guidelines in oncology. Colon Cancer, 3rd edn. pp 1–120
Irland AoCoGBa (2007) Guidelines for the management of colon cancer, 3rd edn
Green BL, Marshall HC, Collinson F, Quirke P, Guillou P, Jayne DG, Brown JM (2013) Long-term follow-up of the Medical Research Council CLASICC trial of conventional versus laparoscopically assisted resection in colorectal cancer. Br J Surg 100(1):75–82. doi:10.1002/bjs.8945
Keshava A, Chapuis PH, Chan C, Lin BP, Bokey EL, Dent OF (2007) The significance of involvement of a free serosal surface for recurrence and survival following resection of clinicopathological stage B and C rectal cancer. Color Dis 9(7):609–618. doi:10.1111/j.1463-1318.2006.01136.x
Gunderson LL, Jessup JM, Sargent DJ, Greene FL, Stewart AK (2010) Revised TN categorization for colon cancer based on national survival outcomes data. J Clin Oncol 28(2):264–271. doi:10.1200/JCO.2009.24.0952
Acknowledgments
The author would like to thank Dr. Maria Clotilde Carra for her help and support in the statistical analysis.
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The study was conducted in accordance with the ethical principles ascertained in the Declaration of Helsinki.
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de’Angelis, N., Vitali, G.C., Brunetti, F. et al. Laparoscopic vs. open surgery for T4 colon cancer: A propensity score analysis . Int J Colorectal Dis 31, 1785–1797 (2016). https://doi.org/10.1007/s00384-016-2646-y
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DOI: https://doi.org/10.1007/s00384-016-2646-y