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Published in: Surgical Endoscopy 2/2019

01-02-2019

Minimally invasive surgery for stage III colon adenocarcinoma is associated with less delay to initiation of adjuvant systemic therapy and improved survival

Authors: Lawrence Lee, Nathalie Wong-Chong, Justin J. Kelly, George J. Nassif, Matthew R. Albert, John R. T. Monson

Published in: Surgical Endoscopy | Issue 2/2019

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Abstract

Background

Minimally invasive surgery (MIS) may improve surgical recovery and reduce time to adjuvant systemic therapy after colon cancer resection. The objective of this study was to determine the effect of MIS on the initiation of adjuvant systemic therapy and survival in patients with stage III colon cancer.

Methods

The 2010–2014 National Cancer Database was queried for patients with resected stage III colon adenocarcinoma, and divided into MIS, which included laparoscopic and robotic approaches, and open surgery. Propensity-score matching was used to balanced open and MIS groups. The main outcome measures were delayed initiation of adjuvant systemic therapy (defined as > 8 weeks after surgery) and 5-year overall survival (OS). Multiple Cox regression was performed to identify independent predictors for 5-year OS, including an interaction between delayed systemic therapy and MIS, and adjusted for clustering at the hospital level.

Results

There were 86,680 patients that were included in this study. Overall, 45% (38,713) underwent MIS colectomy, of which 93% underwent laparoscopic and 7% robotic surgery. After matching, 33,183 open patients were balanced to 33,183 MIS patients. Patient, tumor, and facility characteristics were similar in the matched cohort. More patients in the MIS group received adjuvant therapy within 8 weeks of surgery (49% vs. 42%, p < 0.001), and fewer MIS patients did not receive any systemic therapy (30% vs. 35%, p < 0.001). Delayed initiation of systemic therapy > 8 weeks was associated with worse 5-year OS (HR 1.27, 95%CI 1.19–1.36). MIS was independently associated with improved survival (HR 0.92, 95%CI 0.86–0.97). This relationship remained even if 90-day mortality was excluded.

Conclusions

MIS approaches are associated with less delay to the initiation of adjuvant systemic therapy and improved survival in patients with stage III colon adenocarcinoma. Surgeons should favor MIS approaches for the treatment of stage III colon adenocarcinoma whenever possible.
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Literature
2.
go back to reference Boland GM, Chang GJ, Haynes AB, Chiang YJ, Chagpar R, Xing Y, Hu CY, Feig BW, You YN, Cormier JN (2013) Association between adherence to National Comprehensive Cancer Network treatment guidelines and improved survival in patients with colon cancer. Cancer 119:1593–1601CrossRefPubMed Boland GM, Chang GJ, Haynes AB, Chiang YJ, Chagpar R, Xing Y, Hu CY, Feig BW, You YN, Cormier JN (2013) Association between adherence to National Comprehensive Cancer Network treatment guidelines and improved survival in patients with colon cancer. Cancer 119:1593–1601CrossRefPubMed
3.
go back to reference Booth CM, Nanji S, Wei X, Peng Y, Biagi JJ, Hanna TP, Krzyzanowska MK, Mackillop WJ (2016) Use and effectiveness of adjuvant chemotherapy for stage III colon cancer: a population-based study. J Natl Compr Canc Netw 14:47–56CrossRefPubMed Booth CM, Nanji S, Wei X, Peng Y, Biagi JJ, Hanna TP, Krzyzanowska MK, Mackillop WJ (2016) Use and effectiveness of adjuvant chemotherapy for stage III colon cancer: a population-based study. J Natl Compr Canc Netw 14:47–56CrossRefPubMed
4.
go back to reference Biagi JJ, Raphael MJ, Mackillop WJ, Kong W, King WD, Booth CM (2011) Association between time to initiation of adjuvant chemotherapy and survival in colorectal cancer: a systematic review and meta-analysis. JAMA 305:2335–2342CrossRefPubMed Biagi JJ, Raphael MJ, Mackillop WJ, Kong W, King WD, Booth CM (2011) Association between time to initiation of adjuvant chemotherapy and survival in colorectal cancer: a systematic review and meta-analysis. JAMA 305:2335–2342CrossRefPubMed
5.
go back to reference Becerra AZ, Probst CP, Tejani MA, Aquina CT, Gonzalez MG, Hensley BJ, Noyes K, Monson JR, Fleming FJ (2015) Opportunity lost: adjuvant chemotherapy in patients with stage III colon cancer remains underused. Surgery 158:692–699CrossRefPubMed Becerra AZ, Probst CP, Tejani MA, Aquina CT, Gonzalez MG, Hensley BJ, Noyes K, Monson JR, Fleming FJ (2015) Opportunity lost: adjuvant chemotherapy in patients with stage III colon cancer remains underused. Surgery 158:692–699CrossRefPubMed
6.
go back to reference Lee L, Tran T, Mayo NE, Carli F, Feldman LS (2014) What does it really mean to “recover” from an operation? Surgery 155:211–216CrossRefPubMed Lee L, Tran T, Mayo NE, Carli F, Feldman LS (2014) What does it really mean to “recover” from an operation? Surgery 155:211–216CrossRefPubMed
7.
go back to reference Jin LX, Sanford DE, Squires MH, Moses LE, Yan Y, Poultsides GA, Votanopoulos KI, Weber SM, Bloomston M, Pawlik TM, Hawkins WG, Linehan DC, Schmidt C, Worhunsky DJ, Acher AW, Cardona K, Cho CS, Kooby DA, Levine EA, Winslow E, Saunders N, Spolverato G, Colditz GA, Maithel SK, Fields RC (2016) Interaction of postoperative morbidity and receipt of adjuvant therapy on long-term survival after resection for gastric adenocarcinoma: results from the U.S. Gastric Cancer Collaborative. Ann Surg Oncol 23:2398–2408CrossRefPubMed Jin LX, Sanford DE, Squires MH, Moses LE, Yan Y, Poultsides GA, Votanopoulos KI, Weber SM, Bloomston M, Pawlik TM, Hawkins WG, Linehan DC, Schmidt C, Worhunsky DJ, Acher AW, Cardona K, Cho CS, Kooby DA, Levine EA, Winslow E, Saunders N, Spolverato G, Colditz GA, Maithel SK, Fields RC (2016) Interaction of postoperative morbidity and receipt of adjuvant therapy on long-term survival after resection for gastric adenocarcinoma: results from the U.S. Gastric Cancer Collaborative. Ann Surg Oncol 23:2398–2408CrossRefPubMed
8.
go back to reference Schwenk W, Haase O, Neudecker J, Muller JM (2005) Short term benefits for laparoscopic colorectal resection. Cochrane Database Syst Rev 3::CD003145 Schwenk W, Haase O, Neudecker J, Muller JM (2005) Short term benefits for laparoscopic colorectal resection. Cochrane Database Syst Rev 3::CD003145
9.
go back to reference Dowson HM, Cowie AS, Ballard K, Gage H, Rockall TA (2008) Systematic review of quality of life following laparoscopic and open colorectal surgery. Colorectal Dis 10:757–768CrossRefPubMed Dowson HM, Cowie AS, Ballard K, Gage H, Rockall TA (2008) Systematic review of quality of life following laparoscopic and open colorectal surgery. Colorectal Dis 10:757–768CrossRefPubMed
10.
go back to reference Jung YB, Kang J, Park EJ, Baik SH, Lee KY (2016) Time to initiation of adjuvant chemotherapy in colon cancer: comparison of open, laparoscopic, and robotic surgery. J Laparoendosc Adv Surg Tech A 26:799–805CrossRefPubMed Jung YB, Kang J, Park EJ, Baik SH, Lee KY (2016) Time to initiation of adjuvant chemotherapy in colon cancer: comparison of open, laparoscopic, and robotic surgery. J Laparoendosc Adv Surg Tech A 26:799–805CrossRefPubMed
11.
go back to reference Malietzis G, Mughal A, Currie AC, Anyamene N, Kennedy RH, Athanasiou T, Jenkins JT (2015) Factors implicated for delay of adjuvant chemotherapy in colorectal cancer: a meta-analysis of observational studies. Ann Surg Oncol 22:3793–3802CrossRefPubMed Malietzis G, Mughal A, Currie AC, Anyamene N, Kennedy RH, Athanasiou T, Jenkins JT (2015) Factors implicated for delay of adjuvant chemotherapy in colorectal cancer: a meta-analysis of observational studies. Ann Surg Oncol 22:3793–3802CrossRefPubMed
12.
go back to reference Bilimoria KY, Stewart AK, Winchester DP, Ko CY (2008) The National Cancer Data Base: a powerful initiative to improve cancer care in the United States. Ann Surg Oncol 15:683–690CrossRefPubMedPubMedCentral Bilimoria KY, Stewart AK, Winchester DP, Ko CY (2008) The National Cancer Data Base: a powerful initiative to improve cancer care in the United States. Ann Surg Oncol 15:683–690CrossRefPubMedPubMedCentral
13.
go back to reference Deyo RA, Cherkin DC, Ciol MA (1992) Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol 45:613–619CrossRefPubMed Deyo RA, Cherkin DC, Ciol MA (1992) Adapting a clinical comorbidity index for use with ICD-9-CM administrative databases. J Clin Epidemiol 45:613–619CrossRefPubMed
14.
go back to reference Bos AC, van Erning FN, van Gestel YR, Creemers GJ, Punt CJ, van Oijen MG, Lemmens VE (2015) Timing of adjuvant chemotherapy and its relation to survival among patients with stage III colon cancer. Eur J Cancer 51:2553–2561CrossRefPubMed Bos AC, van Erning FN, van Gestel YR, Creemers GJ, Punt CJ, van Oijen MG, Lemmens VE (2015) Timing of adjuvant chemotherapy and its relation to survival among patients with stage III colon cancer. Eur J Cancer 51:2553–2561CrossRefPubMed
15.
go back to reference Sun Z, Adam MA, Kim J, Nussbaum DP, Benrashid E, Mantyh CR, Migaly J (2016) Determining the optimal timing for initiation of adjuvant chemotherapy after resection for stage II and III colon cancer. Dis Colon Rectum 59:87–93CrossRefPubMed Sun Z, Adam MA, Kim J, Nussbaum DP, Benrashid E, Mantyh CR, Migaly J (2016) Determining the optimal timing for initiation of adjuvant chemotherapy after resection for stage II and III colon cancer. Dis Colon Rectum 59:87–93CrossRefPubMed
16.
go back to reference Des Guetz G, Nicolas P, Perret GY, Morere JF, Uzzan B (2010) Does delaying adjuvant chemotherapy after curative surgery for colorectal cancer impair survival? A meta-analysis. Eur J Cancer 46:1049–1055CrossRefPubMed Des Guetz G, Nicolas P, Perret GY, Morere JF, Uzzan B (2010) Does delaying adjuvant chemotherapy after curative surgery for colorectal cancer impair survival? A meta-analysis. Eur J Cancer 46:1049–1055CrossRefPubMed
17.
go back to reference In H, Bilimoria KY, Stewart AK, Wroblewski KE, Posner MC, Talamonti MS, Winchester DP (2014) Cancer recurrence: an important but missing variable in national cancer registries. Ann Surg Oncol 21:1520–1529CrossRefPubMed In H, Bilimoria KY, Stewart AK, Wroblewski KE, Posner MC, Talamonti MS, Winchester DP (2014) Cancer recurrence: an important but missing variable in national cancer registries. Ann Surg Oncol 21:1520–1529CrossRefPubMed
18.
go back to reference Dehejia RH, S W (1999) Causal effects in nonexperimental studies: reevaluating the evaluation of training programs. J Am Stat Assoc 94:1053–1062CrossRef Dehejia RH, S W (1999) Causal effects in nonexperimental studies: reevaluating the evaluation of training programs. J Am Stat Assoc 94:1053–1062CrossRef
19.
go back to reference Austin PC (2009) Some methods of propensity-score matching had superior performance to others: results of an empirical investigation and Monte Carlo simulations. Biom J Biom Z 51:171–184CrossRef Austin PC (2009) Some methods of propensity-score matching had superior performance to others: results of an empirical investigation and Monte Carlo simulations. Biom J Biom Z 51:171–184CrossRef
20.
go back to reference Flury BK, Reidwyl H (1986) Standard distance in univariate and multivariate analysis. Am Stat 40:249–251 Flury BK, Reidwyl H (1986) Standard distance in univariate and multivariate analysis. Am Stat 40:249–251
21.
go back to reference Austin PC (2009) Using the standardized difference to compare the prevalence of a binary variable between two groups in observational research. Commun Stat Simul Comput 38:1228–1234CrossRef Austin PC (2009) Using the standardized difference to compare the prevalence of a binary variable between two groups in observational research. Commun Stat Simul Comput 38:1228–1234CrossRef
22.
go back to reference Linden A (2017) Improving causal inference with a doubly robust estimator that combines propensity score stratification and weighting. J Eval Clin Pract 23:697–702CrossRefPubMed Linden A (2017) Improving causal inference with a doubly robust estimator that combines propensity score stratification and weighting. J Eval Clin Pract 23:697–702CrossRefPubMed
23.
go back to reference Kim YW, Choi EH, Kim BR, Ko WA, Do YM, Kim IY (2017) The impact of delayed commencement of adjuvant chemotherapy (eight or more weeks) on survival in stage II and III colon cancer: a national population-based cohort study. Oncotarget 8:80061–80072PubMedPubMedCentral Kim YW, Choi EH, Kim BR, Ko WA, Do YM, Kim IY (2017) The impact of delayed commencement of adjuvant chemotherapy (eight or more weeks) on survival in stage II and III colon cancer: a national population-based cohort study. Oncotarget 8:80061–80072PubMedPubMedCentral
24.
go back to reference Becerra AZ, Aquina CT, Mohile SG, Tejani MA, Schymura MJ, Boscoe FP, Xu Z, Justiniano CF, Boodry CI, Swanger AA, Noyes K, Monson JR, Fleming FJ (2017) Variation in delayed time to adjuvant chemotherapy and disease-specific survival in stage III colon cancer patients. Ann Surg Oncol 24:1610–1617CrossRefPubMed Becerra AZ, Aquina CT, Mohile SG, Tejani MA, Schymura MJ, Boscoe FP, Xu Z, Justiniano CF, Boodry CI, Swanger AA, Noyes K, Monson JR, Fleming FJ (2017) Variation in delayed time to adjuvant chemotherapy and disease-specific survival in stage III colon cancer patients. Ann Surg Oncol 24:1610–1617CrossRefPubMed
25.
go back to reference Veenhof AA, Vlug MS, van der Pas MH, Sietses C, van der Peet DL, de Lange-de Klerk ES, Bonjer HJ, Bemelman WA, Cuesta MA (2012) Surgical stress response and postoperative immune function after laparoscopy or open surgery with fast track or standard perioperative care: a randomized trial. Ann Surg 255:216–221CrossRefPubMed Veenhof AA, Vlug MS, van der Pas MH, Sietses C, van der Peet DL, de Lange-de Klerk ES, Bonjer HJ, Bemelman WA, Cuesta MA (2012) Surgical stress response and postoperative immune function after laparoscopy or open surgery with fast track or standard perioperative care: a randomized trial. Ann Surg 255:216–221CrossRefPubMed
26.
go back to reference Xu D, Li J, Song Y, Zhou J, Sun F, Wang J, Duan Y, Hu Y, Liu Y, Wang X, Sun L, Wu L, Ding K (2015) Laparoscopic surgery contributes more to nutritional and immunologic recovery than fast-track care in colorectal cancer. World J Surg Oncol 13::18CrossRef Xu D, Li J, Song Y, Zhou J, Sun F, Wang J, Duan Y, Hu Y, Liu Y, Wang X, Sun L, Wu L, Ding K (2015) Laparoscopic surgery contributes more to nutritional and immunologic recovery than fast-track care in colorectal cancer. World J Surg Oncol 13::18CrossRef
27.
go back to reference King PM, Blazeby JM, Ewings P, Kennedy RH (2008) Detailed evaluation of functional recovery following laparoscopic or open surgery for colorectal cancer within an enhanced recovery programme. Int J Colorectal Dis 23:795–800CrossRefPubMed King PM, Blazeby JM, Ewings P, Kennedy RH (2008) Detailed evaluation of functional recovery following laparoscopic or open surgery for colorectal cancer within an enhanced recovery programme. Int J Colorectal Dis 23:795–800CrossRefPubMed
28.
go back to reference Pecorelli N, Fiore JF Jr, Gillis C, Awasthi R, Mappin-Kasirer B, Niculiseanu P, Fried GM, Carli F, Feldman LS (2016) The six-minute walk test as a measure of postoperative recovery after colorectal resection: further examination of its measurement properties. Surg Endosc 30:2199–2206CrossRefPubMed Pecorelli N, Fiore JF Jr, Gillis C, Awasthi R, Mappin-Kasirer B, Niculiseanu P, Fried GM, Carli F, Feldman LS (2016) The six-minute walk test as a measure of postoperative recovery after colorectal resection: further examination of its measurement properties. Surg Endosc 30:2199–2206CrossRefPubMed
29.
go back to reference Aloia TA, Zimmitti G, Conrad C, Gottumukalla V, Kopetz S, Vauthey JN (2014) Return to intended oncologic treatment (RIOT): a novel metric for evaluating the quality of oncosurgical therapy for malignancy. J Surg Oncol 110:107–114CrossRefPubMedPubMedCentral Aloia TA, Zimmitti G, Conrad C, Gottumukalla V, Kopetz S, Vauthey JN (2014) Return to intended oncologic treatment (RIOT): a novel metric for evaluating the quality of oncosurgical therapy for malignancy. J Surg Oncol 110:107–114CrossRefPubMedPubMedCentral
30.
go back to reference Kim BJ, Caudle AS, Gottumukkala V, Aloia TA (2016) The impact of postoperative complications on a timely return to intended oncologic therapy (RIOT): the role of enhanced recovery in the cancer journey. Int Anesthesiol Clin 54:e33–e46CrossRefPubMed Kim BJ, Caudle AS, Gottumukkala V, Aloia TA (2016) The impact of postoperative complications on a timely return to intended oncologic therapy (RIOT): the role of enhanced recovery in the cancer journey. Int Anesthesiol Clin 54:e33–e46CrossRefPubMed
32.
go back to reference Artinyan A, Orcutt ST, Anaya DA, Richardson P, Chen GJ, Berger DH (2015) Infectious postoperative complications decrease long-term survival in patients undergoing curative surgery for colorectal cancer: a study of 12,075 patients. Ann Surg 261:497–505CrossRefPubMed Artinyan A, Orcutt ST, Anaya DA, Richardson P, Chen GJ, Berger DH (2015) Infectious postoperative complications decrease long-term survival in patients undergoing curative surgery for colorectal cancer: a study of 12,075 patients. Ann Surg 261:497–505CrossRefPubMed
33.
go back to reference McSorley ST, Horgan PG, McMillan DC (2016) The impact of the type and severity of postoperative complications on long-term outcomes following surgery for colorectal cancer: a systematic review and meta-analysis. Crit Rev Oncol Hematol 97:168–177CrossRefPubMed McSorley ST, Horgan PG, McMillan DC (2016) The impact of the type and severity of postoperative complications on long-term outcomes following surgery for colorectal cancer: a systematic review and meta-analysis. Crit Rev Oncol Hematol 97:168–177CrossRefPubMed
34.
go back to reference Di B, Li Y, Wei K, Xiao X, Shi J, Zhang Y, Yang X, Gao P, Zhang K, Yuan Y, Zhang D, Wei X, Liu S, Wang J, Wang X, Zhang Y, Cai H (2013) Laparoscopic versus open surgery for colon cancer: a meta-analysis of 5-year follow-up outcomes. Surg Oncol 22:e39–e43CrossRefPubMed Di B, Li Y, Wei K, Xiao X, Shi J, Zhang Y, Yang X, Gao P, Zhang K, Yuan Y, Zhang D, Wei X, Liu S, Wang J, Wang X, Zhang Y, Cai H (2013) Laparoscopic versus open surgery for colon cancer: a meta-analysis of 5-year follow-up outcomes. Surg Oncol 22:e39–e43CrossRefPubMed
35.
go back to reference Kuhry E, Schwenk WF, Gaupset R, Romild U, Bonjer HJ (2008) Long-term results of laparoscopic colorectal cancer resection. Cochrane Database Syst Rev 2::CD003432 Kuhry E, Schwenk WF, Gaupset R, Romild U, Bonjer HJ (2008) Long-term results of laparoscopic colorectal cancer resection. Cochrane Database Syst Rev 2::CD003432
36.
go back to reference Brooks JM, Ohsfeldt RL (2013) Squeezing the balloon: propensity scores and unmeasured covariate balance. Health Serv Res 48:1487–1507CrossRefPubMed Brooks JM, Ohsfeldt RL (2013) Squeezing the balloon: propensity scores and unmeasured covariate balance. Health Serv Res 48:1487–1507CrossRefPubMed
37.
go back to reference Martel G, Crawford A, Barkun JS, Boushey RP, Ramsay CR, Fergusson DA (2012) Expert opinion on laparoscopic surgery for colorectal cancer parallels evidence from a cumulative meta-analysis of randomized controlled trials. PLoS ONE 7:e35292CrossRefPubMedPubMedCentral Martel G, Crawford A, Barkun JS, Boushey RP, Ramsay CR, Fergusson DA (2012) Expert opinion on laparoscopic surgery for colorectal cancer parallels evidence from a cumulative meta-analysis of randomized controlled trials. PLoS ONE 7:e35292CrossRefPubMedPubMedCentral
38.
go back to reference Akmal Y, Bailey C, Baek JH, Metchikian M, Pigazzi A (2011) Oncological outcomes of laparoscopic colon resection for cancer after implementation of a full-time preceptorship. Surg Endosc 25:2967–2971CrossRefPubMed Akmal Y, Bailey C, Baek JH, Metchikian M, Pigazzi A (2011) Oncological outcomes of laparoscopic colon resection for cancer after implementation of a full-time preceptorship. Surg Endosc 25:2967–2971CrossRefPubMed
39.
go back to reference Park EJ, Kim MS, Kim G, Kim CH, Hur H, Min BS, Baik SH, Lee KY, Kim NK (2015) Long-term oncologic outcomes of laparoscopic right hemicolectomy during the learning curve period: comparative study with cases after the learning curve period. Surg Laparosc Endosc Percutan Tech 25:52–58CrossRefPubMed Park EJ, Kim MS, Kim G, Kim CH, Hur H, Min BS, Baik SH, Lee KY, Kim NK (2015) Long-term oncologic outcomes of laparoscopic right hemicolectomy during the learning curve period: comparative study with cases after the learning curve period. Surg Laparosc Endosc Percutan Tech 25:52–58CrossRefPubMed
40.
go back to reference Panchal JM, Lairson DR, Chan W, Du XL (2016) Geographic variation in oxaliplatin chemotherapy and survival in patients with colon cancer. Am J Ther 23:e720–e729CrossRefPubMed Panchal JM, Lairson DR, Chan W, Du XL (2016) Geographic variation in oxaliplatin chemotherapy and survival in patients with colon cancer. Am J Ther 23:e720–e729CrossRefPubMed
41.
go back to reference Morris M, Platell C, Fritschi L, Iacopetta B (2007) Failure to complete adjuvant chemotherapy is associated with adverse survival in stage III colon cancer patients. Br J Cancer 96:701–707CrossRefPubMedPubMedCentral Morris M, Platell C, Fritschi L, Iacopetta B (2007) Failure to complete adjuvant chemotherapy is associated with adverse survival in stage III colon cancer patients. Br J Cancer 96:701–707CrossRefPubMedPubMedCentral
42.
go back to reference Bailey MB, Davenport DL, Vargas HD, Evers BM, McKenzie SP (2014) Longer operative time: deterioration of clinical outcomes of laparoscopic colectomy versus open colectomy. Dis Colon Rectum 57:616–622CrossRefPubMed Bailey MB, Davenport DL, Vargas HD, Evers BM, McKenzie SP (2014) Longer operative time: deterioration of clinical outcomes of laparoscopic colectomy versus open colectomy. Dis Colon Rectum 57:616–622CrossRefPubMed
43.
go back to reference Curtis NJ, Taylor M, Fraser L, Salib E, Noble E, Hipkiss R, Allison AS, Dalton R, Ockrim JB, Francis NK (2017) Can the combination of laparoscopy and enhanced recovery improve long-term survival after elective colorectal cancer surgery? Int J Colorectal Dis 33(2):231–234CrossRefPubMed Curtis NJ, Taylor M, Fraser L, Salib E, Noble E, Hipkiss R, Allison AS, Dalton R, Ockrim JB, Francis NK (2017) Can the combination of laparoscopy and enhanced recovery improve long-term survival after elective colorectal cancer surgery? Int J Colorectal Dis 33(2):231–234CrossRefPubMed
Metadata
Title
Minimally invasive surgery for stage III colon adenocarcinoma is associated with less delay to initiation of adjuvant systemic therapy and improved survival
Authors
Lawrence Lee
Nathalie Wong-Chong
Justin J. Kelly
George J. Nassif
Matthew R. Albert
John R. T. Monson
Publication date
01-02-2019
Publisher
Springer US
Published in
Surgical Endoscopy / Issue 2/2019
Print ISSN: 0930-2794
Electronic ISSN: 1432-2218
DOI
https://doi.org/10.1007/s00464-018-6319-5

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