Effects of neoadjuvant chemotherapy plus chemoradiotherapy on lymph nodes in rectal adenocarcinoma.
Adenocarcinoma
/ therapy
Adult
Aged
Antineoplastic Combined Chemotherapy Protocols
/ therapeutic use
Chemoradiotherapy
/ methods
Female
France
/ epidemiology
Humans
Lymph Node Excision
Lymph Nodes
/ drug effects
Male
Middle Aged
Neoadjuvant Therapy
/ methods
Neoplasm Staging
Rectal Neoplasms
/ physiopathology
Rectum
/ pathology
Retrospective Studies
Induction chemotherapy
Lymph node
Radiochemotherapy
Rectal cancer
Total neoadjuvant treatment
Journal
Virchows Archiv : an international journal of pathology
ISSN: 1432-2307
Titre abrégé: Virchows Arch
Pays: Germany
ID NLM: 9423843
Informations de publication
Date de publication:
Oct 2021
Oct 2021
Historique:
received:
13
02
2021
accepted:
21
04
2021
revised:
13
04
2021
pubmed:
14
5
2021
medline:
29
10
2021
entrez:
13
5
2021
Statut:
ppublish
Résumé
The pathological nodal stage, determination of which requires examination of ≥ 12 lymph nodes, is one of the main prognostic factors in rectal cancer. Neoadjuvant chemoradiotherapy (CRT) may reduce the number of both lymph nodes retrieved and positive lymph nodes. Induction chemotherapy before CRT aimed at reducing the rate of distant metastases. However, the impact of this new treatment on number of lymph nodes retrieved and positive lymph nodes is unknown. This study was performed to evaluate the effects of neoadjuvant chemotherapy on lymph nodes in locally advanced rectal cancer treated by CRT. We retrospectively included patients with T2 - 4 Nx M0 rectal cancer and compared those receiving neoadjuvant chemotherapy plus CRT with those receiving CRT alone. From 2012 to 2019, 85 patients were treated with neoadjuvant chemotherapy + CRT and 189 with CRT alone. The number of lymph nodes retrieved (19 vs. 17, respectively, P = 0.434), the rate of specimens with ≥ 12 lymph nodes (92% vs. 88%, respectively, P = 0.397), and the median number of positive lymph nodes (1 vs. 2, respectively, P = 0.878) were similar between the two groups. However, the rate of pN0 was higher after neoadjuvant chemotherapy + CRT compared to CRT (75% vs. 62%, respectively, P = 0.030). Neoadjuvant chemotherapy before CRT for locally advanced rectal cancer did not modify the number of lymph nodes retrieved or the number of positive lymph nodes compared to CRT alone. However, it significantly increased the rate of tumors without any positive lymph nodes (ypN0).
Identifiants
pubmed: 33983519
doi: 10.1007/s00428-021-03108-3
pii: 10.1007/s00428-021-03108-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
657-666Informations de copyright
© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Brierley JD, Gospodarowicz MK, Wittekinf C (eds) (2017) TNM Classification of Malignant Tumors, 8th edn. Wiley-Blackwell, Oxford
Duchalais E, Glyn Mullaney T, Spears GM, Kelley SR, Mathis K, Harmsen WS, Larson DW (2018) Prognostic value of pathological node status after neoadjuvant radiotherapy for rectal cancer. Br J Surg 105:1501–1509. https://doi.org/10.1002/bjs.10867
doi: 10.1002/bjs.10867
pubmed: 29663352
Swanson RS, Compton CC, Stewart AK, Bland KI (2003) The prognosis of T3N0 colon cancer is dependent on the number of lymph nodes examined. Ann Surg Oncol 10:65–71. https://doi.org/10.1245/aso.2003.03.058
doi: 10.1245/aso.2003.03.058
pubmed: 12513963
Kakar S, Shi C, Berho ME et al (2017) Protocol for the examination of specimens from patients with primary carcinoma of the colon and rectum. https://documents.cap.org/protocols/cp-gilower-colonrectum-17protocol-4010.pdf
Loughrey MB, Quirke P, Shepherd NA (2018) Standards and datasets for reporting cancers Dataset for colorectal cancer histopathology reports. https://www.rcpath.org/search-results.html?q=G049+Dataset+for+histopathological+reporting+of+colorectal+cancer
Raoof M, Zafar SN, Ituarte PHG, Krouse RS, Melstrom K (2019) Using a lymph node count metric to identify underperforming hospitals after rectal cancer surgery. J Surg Res 236:216–223. https://doi.org/10.1016/j.jss.2018.11.040
doi: 10.1016/j.jss.2018.11.040
pubmed: 30694758
Morris EJA, Maughan NJ, Forman D, Quirke P (2007) Identifying stage III colorectal cancer patients: the influence of the patient, surgeon, and pathologist. J Clin Oncol 25:2573–2579. https://doi.org/10.1200/JCO.2007.11.0445
doi: 10.1200/JCO.2007.11.0445
pubmed: 17577036
Mechera R, Schuster T, Rosenberg R, Speich B (2017) Lymph node yield after rectal resection in patients treated with neoadjuvant radiation for rectal cancer: a systematic review and meta-analysis. Eur J Cancer 72:8–94. https://doi.org/10.1016/j.ejca.2016.10.031
doi: 10.1016/j.ejca.2016.10.031
Yegen G, Keskin M, Büyük M, Kunduz E, Balık E, Sağlam EK, Kapran Y, Asoğlu O, Güllüoğlu M (2016) The effect of neoadjuvant therapy on the size, number, and distribution of mesorectal lymph nodes. Ann Diagn Pathol 20:29–35. https://doi.org/10.1016/j.anndiagpath.2015.10.008
doi: 10.1016/j.anndiagpath.2015.10.008
pubmed: 26706785
Gérard JP, André T, Bibeau F, Conroy T, Legoux JL, Portier G, Bosset JF, Cadiot G, Bouché O, Bedenne L (2017) Rectal cancer: French Intergroup clinical practice guidelines for diagnosis, treatments and follow-up. Dig Liver Dis 49:359–367. https://doi.org/10.1016/j.dld.2017.01.152
doi: 10.1016/j.dld.2017.01.152
pubmed: 28179091
Peeters KC, Marijnen CA, Nagtegaal ID, Kranenbarg EK, Putter H, Wiggers T, Rutten H, Pahlman L, Glimelius B, Leer JW, van de Velde CJH, Dutch Colorectal Cancer Group (2007) The TME trial after a median follow-up of 6 years: increased local control but no survival benefit in irradiated patients with resectable rectal. Ann Surg 246:693–701. https://doi.org/10.1097/01.sla.0000257358.56863.ce
doi: 10.1097/01.sla.0000257358.56863.ce
pubmed: 17968156
Bujko K, Glimelius B, Valentini V, Wi M, Spalek M (2015) Postoperative chemotherapy in patients with rectal cancer receiving preoperative radio(chemo)therapy: a meta-analysis of randomized trials comparing surgery ± a fluoropyrimidine and surgery + a fluoropyrimidine ± oxaliplatin. Eur J Surg Oncol 41:713–723. https://doi.org/10.1016/j.ejso.2015.03.233
doi: 10.1016/j.ejso.2015.03.233
pubmed: 25911110
Breugom AJ, Swets M, Bosset JF, Collette L, Sainato A, Cionini L, Glynne-Jones R, Counsell N, Bastiaannet E, van den Broek CBM, Liefers GJ, Putter H, van de Velde CJH (2015) Adjuvant chemotherapy after preoperative (chemo)radiotherapy and surgery for patients with rectal cancer: a systematic review and meta-analysis of individual patient data. Lancet Oncol 16:200–207. https://doi.org/10.1016/S1470-2045(14)71199-4
doi: 10.1016/S1470-2045(14)71199-4
pubmed: 25589192
Conroy T, Lamfichekh N, Etienne PL, Rio E, Francois E, Mesgouez-Nebout N, Vendrely V, Artignan X, Bouché O, Gargot D, Boige V, Bonichon-Lamichhane N, Louvet C, Morand C, De La Fouchardiere C, Juzyna B, Rullier E, Marchal F, Castan F, Borg C (2020) Total neoadjuvant therapy with mFOLFIRINOX versus preoperative chemoradiation in patients with locally advanced rectal cancer: Final results of PRODIGE 23 phase III trial, a UNICANCER GI trial. J Clin Oncol 38 (suppl; abstr 4007). https://doi.org/10.1200/JCO.2020.38.15
Dewdney A, Cunningham D, Tabernero J, Capdevila J, Glimelius B, Cervantes A, Tait D, Brown G, Wotherspoon A, Gonzalez de Castro D, Chua YJ, Wong R, Barbachano Y, Oates J, Chau I (2012) Multicenter randomized phase II clinical trial comparing neoadjuvant oxaliplatin, capecitabine, and preoperative radiotherapy with or without cetuximab followed by total mesorectal excision in patients with high-risk rectal cancer (EXPERT-C). J Clin Oncol 30:1620–1627. https://doi.org/10.1200/JCO.2011.39.6036
doi: 10.1200/JCO.2011.39.6036
pubmed: 22473163
Fernandez-Martos C, Garcia-Albeniz X, Pericay C, Maurel J, Aparicio J, Montagut C, Safont MJ, Salud A, Vera R, Massuti B, Escudero P, Alonso V, Bosch C, Martin M, Minsky BD (2015) Chemoradiation, surgery and adjuvant chemotherapy versus induction chemotherapy followed by chemoradiation and surgery: long-term results of the Spanish GCR-3 phase II randomized trial. Ann Oncol 26:1722–1728. https://doi.org/10.1093/annonc/mdv223
doi: 10.1093/annonc/mdv223
pubmed: 25957330
Schou JV, Larsen FO, Rasch L, Linnemann D, Langhoff J, Høgdall E, Nielsen DL, Vistisen K, Fromm A, Jensen BV (2012) Induction chemotherapy with capecitabine and oxaliplatin followed by chemoradiotherapy before total mesorectal excision in patients with locally advanced rectal cancer. Ann Oncol 23:2627–2633. https://doi.org/10.1093/annonc/mds056
doi: 10.1093/annonc/mds056
pubmed: 22473488
Gollins S, West N, Sebag-Montefiore D, Susnerwala S, Falk S, Brown N, Saunders M, Quirke P, Ray R, Parsons P, Griffiths G, Maughan T, Adams R, Hurt C (2018) A prospective phase II study of pre-operative chemotherapy then short-course radiotherapy for high risk rectal cancer: COPERNICUS. Br J Cancer 119:697–706. https://doi.org/10.1038/s41416-018-0209-4
doi: 10.1038/s41416-018-0209-4
pubmed: 30116024
pmcid: 6173784
Chua YJ, Barbachano Y, Cunningham D, Oates JR, Brown G, Wotherspoon A, Tait D, Massey A, Tebbutt NC, Chau I (2010) Neoadjuvant capecitabine and oxaliplatin before chemoradiotherapy and total mesorectal excision in MRI-defined poor-risk rectal cancer: a phase 2 trial. Lancet Oncol 11:241–248. https://doi.org/10.1016/S1470-2045(09)70381-X
doi: 10.1016/S1470-2045(09)70381-X
pubmed: 20106720
Dueland S, Ree AH, Grøholt KK, Saelen MG, Folkvord S, Hole KH, Seiersta T, Larsen SG, Giercksky KE, Wiig JN, Boye K, Flatmark K (2016) Oxaliplatin-containing preoperative therapy in locally advanced rectal cancer: local response, toxicity and long-term outcome. Clin Oncol 28:532–539. https://doi.org/10.1016/j.clon.2016.01.014
doi: 10.1016/j.clon.2016.01.014
Cercek A, Goodman KA, Hajj C, Weisberger E, Segal NH, Reidy-Lagunes DL, Stadler ZK, Wu AJ, Weiser MR, Paty PB, Guillem JG, Nash GM, Temple LK, Garcia-Aguilar J, Saltz LB (2014) Neoadjuvant chemotherapy first, followed by chemoradiation and then surgery, in the management of locally advanced rectal cancer. J Natl Compr Canc Netw 12:513–519. https://doi.org/10.6004/jnccn.2014.0056
doi: 10.6004/jnccn.2014.0056
pubmed: 24717570
pmcid: 5612781
Cercek A, Roxburgh CSD, Strombom P, Smith JJ, Temple LKF, Nash GM, Guillem JG, Paty PB, Yaeger R, Stadler ZK, Seier K, Gonen M, Segal NH, Reidy DL, Varghese A, Shia J, Vakiani E, Wu AJ, Crane CH, Gollub MJ, Garcia-Aguilar J, Saltz LB, Weiser MR (2018) Adoption of total neoadjuvant therapy for locally advanced rectal cancer. JAMA Oncol 4:e180071. https://doi.org/10.1001/jamaoncol.2018.0071
doi: 10.1001/jamaoncol.2018.0071
pubmed: 29566109
pmcid: 5885165
Fokas E, Allgäuer M, Polat B, Klautke G, Grabenbauer GG, Fietkau R, Kuhnt T, Staib L, Brunner T, Grosu AL, Schmiegel W, Jacobasch L, Weitz J, Folprecht G, Schlenska-Lange A, Flentje M, Germer CT, Grützmann R, Schwarzbach M, Paolucci V, Bechstein WO, Friede T, Ghadimi M, Hofheinz RD, Rödel C, German Rectal Cancer Study Group (2019) Randomized phase II trial of chemoradiotherapy plus induction or consolidation chemotherapy as total neoadjuvant therapy for locally advanced rectal cancer: CAO/ARO/AIO-12. J Clin Oncol 37:3212–3222. https://doi.org/10.1200/JCO.19.00308
doi: 10.1200/JCO.19.00308
pubmed: 31150315
Garcia-Aguilar J, Patil S, Kim JK, Yuval JB, Thompson H, Verheij F, Lee M, Saltz LB, On behalf of the OPRA Consortium (2020) Preliminary results of the organ preservation of rectal adenocarcinoma (OPRA) trial. J Clin Oncol 38 (suppl; abstr 4008). https://doi.org/10.1200/JCO.2020.38.15
Garcia-Aguilar J, Chow OS, Smith DD, Marcet JE, Cataldo PA, Varma MG, Kumar AS, Oommen S, Coutsoftides T, Hunt SR, Stamos MJ, Ternent CA, Herzig DO, Fichera A, Polite BN, Dietz DW, Patil S, Avila K, Timing of Rectal Cancer Response to Chemoradiation Consortium (2015) Effect of adding mFOLFOX6 after neoadjuvant chemoradiation in locally advanced rectal cancer: a multicentre, phase 2 trial. Lancet Oncol 16:957–966. https://doi.org/10.1016/S1470-2045(15)00004-2
doi: 10.1016/S1470-2045(15)00004-2
pubmed: 26187751
pmcid: 4670237
Bujko K, Wyrwicz L, Rutkowski A, Malinowska M, Pietrzak L, Kryński J, Michalski W, Olędzki J, Kuśnierz J, Zając L, Bednarczyk M, Szczepkowski M, Tarnowski W, Kosakowska E, Zwoliński J, Winiarek M, Wiśniowska K, Partycki M, Bęczkowska K, Polkowski W, Styliński R, Wierzbicki R, Bury P, Jankiewicz M, Paprota K, Lewicka M, Ciseł B, Skórzewska M, Mielko J, Bębenek M, Maciejczyk A, Kapturkiewicz B, Dybko A, Hajac Ł, Wojnar A, Leśniak T, Zygulska J, Jantner D, Chudyba E, Zegarski W, Las-Jankowska M, Jankowski M, Kołodziejski L, Radkowski A, Żelazowska-Omiotek U, Czeremszyńska B, Kępka L, Kolb-Sielecki J, Toczko Z, Fedorowicz Z, Dziki A, Danek A, Nawrocki G, Sopyło R, Markiewicz W, Kędzierawski P, Wydmański J, Polish Colorectal Study Group (2016) Long-course oxaliplatin-based preoperative chemoradiation versus 5 × 5 Gy and consolidation chemotherapy for cT4 or fixed cT3 rectal cancer: results of a randomized phase III study. Ann Oncol 27:834–842. https://doi.org/10.1093/annonc/mdw062
doi: 10.1093/annonc/mdw062
pubmed: 26884592
Zhu J, Gu W, Lian P, Sheng W, Cai G, Shi D, Cai S, Zhang Z (2013) A phase II trial of neoadjuvant IMRT-based chemoradiotherapy followed by one cycle of capecitabine for stage II/III rectal adenocarcinoma. Radiat Oncol 8:130–137. https://doi.org/10.1186/1748-717X-8-130
doi: 10.1186/1748-717X-8-130
pubmed: 23718210
pmcid: 3680166
van der Valk MJM, Marijnen CAM, van Etten B, Dijkstra EA, Hilling DE, Kranenbarg EMK, Putter H, Roodvoets AGH, Bahadoer RR, Fokstuen T, Tije AJT, Capdevila J, Hendriks MP, Edhemovic I, Cervantes AMR, de Groot DJA, Nilsson PJ, Glimelius B, van de Velde CJH, Hospers GAP, Collaborative investigators, (2020) Compliance and tolerability of short-course radiotherapy followed by preoperative chemotherapy and surgery for high-risk rectal cancer — results of the international randomized RAPIDO-trial. Radiother Oncol 147:75–83. https://doi.org/10.1016/j.radonc.2020.03.011
doi: 10.1016/j.radonc.2020.03.011
pubmed: 32240909
Bahadoer RR, Dijkstra EA, van Etten B, Marijnen CAM, Putter H, Kranenbarg EM, Roodvoets AGH, Nagtegaal ID, Beets-Tan RGH, Blomqvist LK, Fokstuen T, Ten Tije AJ, Capdevila J, Hendriks MP, Edhemovic I, Cervantes A, Nilsson PJ, Glimelius B, van de Velde CJH, Hospers GAP, RAPIDO collaborative investigators. (2021) Short-course radiotherapy followed by chemotherapy before total mesorectal excision (TME) versus preoperative chemoradiotherapy, TME, and optional adjuvant chemotherapy in locally advanced rectal cancer (RAPIDO): a randomised, open-label, phase 3 trial. Lancet Oncol 22:29–42. https://doi.org/10.1016/S1470-2045(20)30555-6
doi: 10.1016/S1470-2045(20)30555-6
pubmed: 33301740
Gao YH, Lin JZ, An X, Luo JL, Cai MY, Cai PQ, Kong LH, Liu GC, Tang JH, Chen G, Pan ZZ, Ding PR (2014) Neoadjuvant sandwich treatment with oxaliplatin and capecitabine administered prior to, concurrently with, and following radiation therapy in locally advanced rectal cancer: a prospective phase 2 trial. Int J Radiat Oncol Biol Phys 90:1153–1160. https://doi.org/10.1016/j.ijrobp.2014.07.021
doi: 10.1016/j.ijrobp.2014.07.021
pubmed: 25442042
Rullier E, Rouanet P, Tuech JJ, Valverde A, Lelong B, Rivoire M, Faucheron JL, Jafari M, Portier G, Meunier B, Sileznieff Z, Prudhomme M, Marchal F, Pocard M, Pezet D, Rullier A, Vendrely V, Denost Q, Asselineau J, Doussau A (2017) Organ preservation for rectal cancer (GRECCAR 2): a prospective, randomised, open-label, multicentre, phase 3 trial. Lancet 390:469–479. https://doi.org/10.1016/S0140-6736(17)31056-5
doi: 10.1016/S0140-6736(17)31056-5
pubmed: 28601342
Habr-Gama A, São Julião GP, Vailati BB, Sabbaga J, Aguilar PB, Fernandez LM, Araújo SEA, Perez RO (2019) Organ preservation in cT2N0 rectal cancer after neoadjuvant chemoradiation therapy: the impact of radiation therapy dose-escalation and consolidation chemotherapy. Ann Surg 269:102–107. https://doi.org/10.1097/SLA.0000000000002447
doi: 10.1097/SLA.0000000000002447
pubmed: 28742703
Bridoux V, de Chaisemartin C, Beyer L, Goasguen N, Sabbagh C, Guedj N, Dartigues P, Bardier A (2016) Recommandations pour la pratique clinique. Cancer du rectum. Question 2: Quels sont les critères de qualité de l’exérèse hirurgicale? Colon Rectum 10:12–27. https://doi.org/10.1007/s11725-015-0617-z
doi: 10.1007/s11725-015-0617-z
Manceau G, Margot N, Augustin J, Bardier A, Simon JM, Bachet JB, Spano JP, Maingon P, Vaillant JC, Karoui M (2020) YpN0 rectal cancer patients with sterilized lymph nodes after neoadjuvant chemoradiotherapy are of greater risk of recurrence. Dig Liver Dis 52:214–220. https://doi.org/10.1016/j.dld.2019.07.013
doi: 10.1016/j.dld.2019.07.013
pubmed: 31427089
Ryan R, Gibbons D, Hyland JM, Treanor D, White A, Mulcahy HE, O’Donoghue DP, Moriarty M, Fennelly D, Sheahan K (2005) Pathological response following long-course neoadjuvant chemoradiotherapy for locally advanced rectal cancer. Histopathology 47:141–146. https://doi.org/10.1111/j.1365-2559.2005.02176.x
doi: 10.1111/j.1365-2559.2005.02176.x
pubmed: 16045774
Rullier A, Laurent C, Capdepont M, Vendrely V, Belleannée G, Bioulac-Sage P, Rullier E (2008) Lymph nodes after preoperative chemoradiotherapy for rectal carcinoma: number, status, and impact on survival. Am J Surg Pathol 32:45–50. https://doi.org/10.1097/pas.0b013e3180dc92ab
doi: 10.1097/pas.0b013e3180dc92ab
pubmed: 18162769
Degiuli M, Arolfo S, Evangelista A, Lorenzon L, Reddavid R, Staudacher C, De Nardi P, Rosati R, Elmore U, Coco C, Rizzo G, Belluco C, Forlin M, Milone M, Domenico De Palma G, Rega D, Delrio P, Guerrieri M, Ortenzi M, Muratore A, Marsanic P, Restivo A, Deidda S, Zuin M, Pucciarelli S, De Luca R, Persiani R, Biondi A, Roviello F, Marelli D, Sgroi G, Turati L, Morino M (2018) Number of lymph nodes assessed has no prognostic impact in node-negative rectal cancers after neoadjuvant therapy. Results of the “Italian Society of Surgical Oncology (S.I.C.O.) Colorectal Cancer Network” (SICO-CCN) multicentre collaborative study. Eur J Surg Oncol 44:1233–1240. https://doi.org/10.1016/j.ejso.2018.04.007
doi: 10.1016/j.ejso.2018.04.007
pubmed: 29705284
Marks JH, Valsdottir EB, Rather AA, Nweze IC, Newman DA, Chernick MR (2010) Fewer than 12 lymph nodes can be expected in a surgical specimen after high-dose chemoradiation therapy for rectal cancer. Dis Colon Rectum 53:1023–1029. https://doi.org/10.1007/dcr.0b013e3181dadeb4
doi: 10.1007/dcr.0b013e3181dadeb4
pubmed: 20551754
Gao P, Song Y, Yang Y, Zhao S, Sun Y, Sun J, Chen X, Wang Z (2018) What is the minimum number of examined lymph nodes after neoadjuvant therapy in rectal cancer? J Gastrointest Surg 22:1068–1076. https://doi.org/10.1007/s11605-018-3717-x
doi: 10.1007/s11605-018-3717-x
pubmed: 29468556
Gurawalia J, Dev K, Nayak SP, Kurpad V, Pandey A (2016) Less than 12 lymph nodes in the surgical specimen after neoadjuvant chemo-radiotherapy: an indicator of tumor regression in locally advanced rectal cancer? J Gastrointest Oncol 7:946–957. https://doi.org/10.21037/jgo.2016.09.03
doi: 10.21037/jgo.2016.09.03
pubmed: 28078118
pmcid: 5177569
Bustamante-Lopez LA, Nahas CSR, Nahas SC, Marques CSF, Pinto RA, Cotti GC, Imperiale AR, Sobroza de Mello E, Ribeiro U Jr, Cecconello I (2018) Pathologic complete response implies a fewer number of lymph nodes in specimen of rectal cancer patients treated by neoadjuvant therapy and total mesorectal excision. Int J Surg 56:283–287. https://doi.org/10.1016/j.ijsu.2018.07.001
doi: 10.1016/j.ijsu.2018.07.001
pubmed: 29981939
Wang Y, Zhou M, Yang J, Sun X, Zou W, Zhang Z, Zhang J, Shen L, Yang L, Zhang Z (2019) Increased lymph node yield indicates improved survival in locally advanced rectal cancer treated with neoadjuvant chemoradiotherapy. Cancer Med 8:4615–4625. https://doi.org/10.1002/cam4.2372
doi: 10.1002/cam4.2372
pubmed: 31250569
pmcid: 6712464
Boutanos C, Capdepont M, Svrcek M, Thélu F, Guedj N, Poizat F, Bibeau F, Turlin B, Rousseau A, Bardier A, Selves J, Desrousseaux M, Le Pessot F, Bonhomme B, Laverrière MH, Julié C, Eyremandi RP, Stanislas S, Bazille C, Daubech A, Lazure T, Bordier MS, Demoures A, Rullier A (2019) National multicentric evaluation of quality of pathology reports for rectal cancer in France in 2016. Virchows Arch 474:561–568. https://doi.org/10.1007/s00428-019-02534-8
doi: 10.1007/s00428-019-02534-8
pubmed: 30729335