Abstract
Different guidelines for colorectal cancer (CRC) pathology reporting have been published. We aimed to identify differences between publicly available CRC reporting guidelines and to survey pathologists from different countries to establish the degree of guideline implementation in local routine practice. We compared all core and non-core items of CRC reporting guidelines to identify discrepancies. We then created a survey, which was sent out to 782 pathologists practicing in 30 different countries. It included questions on the demographics of the reporting pathologist as well as resection specimen handling and microscopic evaluation, grading, staging, and additional techniques, such as immunohistochemistry or molecular pathology. First, core and non-core items of five national CRC reporting guidelines were compared and 12 items were found to differ. Different items are considered core or non-core by different guidelines and more than one TNM staging edition was applied across guidelines. The survey was completed by 143 pathologists from 30 countries. We identified differences between local practice and guidelines with potential clinical impact, e.g., tumor budding was never reported by 28.7% of responders, although it has prognostic value for survival in stage II CRC. This is the first international study comparing CRC pathology reporting guidelines with real-world local practices. There are differences in CRC pathology reporting guidelines and in guideline implementation into local practice, both with potential impact on patient care. Harmonization of datasets, use of templates, and audits of local pathology practice are needed to ensure best possible quality of CRC pathology reporting.
Similar content being viewed by others
References
Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386. https://doi.org/10.1002/ijc.29210
Nakhleh RE (2011) Quality in surgical pathology communication and reporting. Arch Pathol Lab Med 135:1394–1397
Dataset for colorectal cancer histopathology reports (3rd edition). https://www.rcpath.org/resourceLibrary/dataset-for-colorectal-cancer-histopathology-reports%2D%2D3rd-edition-.html. Accessed December 7, 2017
Tang LH, Branton P, Burgart LJ et al (2016) Protocol for the examination of specimens from patients with primary carcinoma of the colon and rectum. Accessed December 7, 2017
Obaseki D (2015) An audit of colorectal cancer histopathology reports in a tertiary health care center in Nigeria. Niger J Gastroenterol Hepatol 7:19–24
Nambiar A, Vivek N, Bindu MR, Sudheer OV, Bai L (2010) Completeness of low anterior resection pathology report: a hospital-based audit with recommendations on improving reporting. Indian J Cancer 47:156–159. https://doi.org/10.4103/0019-509X.63010
Messenger DE, McLeod RS, Kirsch R (2011) What impact has the introduction of a synoptic report for rectal cancer had on reporting outcomes for specialist gastrointestinal and nongastrointestinal pathologists? Arch Pathol Lab Med 135:1471–1475. https://doi.org/10.5858/arpa.2010-0558-OA
Chan NG, Duggal A, Weir MM, Driman DK (2008) Pathological reporting of colorectal cancer specimens: a retrospective survey in an academic Canadian pathology department. Can J Surg 51:284–288
Cross SS, Feeley KM, Angel CA (1998) The effect of four interventions on the informational content of histopathology reports of resected colorectal carcinomas. J Clin Pathol 51:481–482
Woods YL, Mukhtar S, McClements P, Lang J, Steele RJ, Carey FA (2014) A survey of reporting of colorectal cancer in Scotland: compliance with guidelines and effect of proforma reporting. J Clin Pathol 67:499–505. https://doi.org/10.1136/jclinpath-2013-202060
Olszyna-Serementa M, Kołodziejczyk M, Sprawka A, Nasierowska-Guttmejer A, Bujko K (2009) The quality of pathological reports of postoperative specimens in rectal cancer: an audit from the Mazovia region. Pol J Pathol 60:130–133
Eon Y, Le Douy J-Y, Lamer B, Battini J, Bretagne J-F (2006) Quality and completeness of histopathology reports of rectal cancer resections. Results of an audit in Brittany. Gastroenterol Clin Biol 30:235–240
Bull AD, Biffin AH, Mella J, Radcliffe AG, Stamatakis JD, Steele RJ, Williams GT (1997) Colorectal cancer pathology reporting: a regional audit. J Clin Pathol 50:138–142
Chapuis PH, Chan C, Lin BPC, Armstrong K, Armstrong B, Spigelman AD, O’Connell D, Leong D, Dent OF (2007) Pathology reporting of resected colorectal cancers in New South Wales. ANZ J Surg 77:963–969. https://doi.org/10.1111/j.1445-2197.2007.04291.x
Winn RD, Robinson DR, Farmer KC, Bell SW (2008) Deficiencies in pathological reporting of colorectal cancer in Victoria. ANZ J Surg 78:796–799. https://doi.org/10.1111/j.1445-2197.2008.04653.x
Idowu MO, Bekeris LG, Raab S, Ruby SG, Nakhleh RE (2010) Adequacy of surgical pathology reporting of cancer: a College of American Pathologists Q-Probes study of 86 institutions. Arch Pathol Lab Med 134:969–974. https://doi.org/10.1043/2009-0412-CP.1
Srigley J, Lankshear S, Brierley J, McGowan T, Divaris D, Yurcan M, Rossi R, Yardley T, King MJ, Ross J, Irish J, McLeod R, Sawka C (2013) Closing the quality loop: facilitating improvement in oncology practice through timely access to clinical performance indicators. J Oncol Pract 9:e255–e261. https://doi.org/10.1200/JOP.2012.000818
Haugland HK, Casati B, Dørum LM, Bjugn R (2011) Template reporting matters - a nationwide study on histopathology reporting on colorectal carcinoma resections. Hum Pathol 42:36–40. https://doi.org/10.1016/j.humpath.2010.06.009
Keating J, Lolohea S, Kenwright D (2003) Pathology reporting of rectal cancer: a national audit. N Z Med J 116:U514
Colorectal Cancer Structured Reporting Protocol (3rd Edition 2016) https://www.rcpa.edu.au/Library/Practising-Pathology/Structured-Pathology-Reporting-of-Cancer/Cancer-Protocols/Gastrointestinal/Protocol-colorectal-cancer. Accessed December 7, 2017
Libro Blanco de la Anatomía Patológica en España 2017 https://www.seap.es/documents/10157/1546214/LBAP_2017+-.pdf/c3fcb02b-3b08-4e6c-bbac-eda437485dc6. Accessed December 7, 2017
Lanza G, Messerini L, Gafà R, Risio M, Gruppo Italiano Patologi Apparato Digerente (GIPAD), Società Italiana di Anatomia Patologica e Citopatologia Diagnostica/International Academy of Pathology, Italian division (SIAPEC/IAP) (2011) Colorectal tumors: the histology report. Dig Liver Dis 43:S344–S355. https://doi.org/10.1016/S1590-8658(11)60590-2
Loughrey MB, Quirke P, Shepherd NA (2017) G049 Dataset for histopathological reporting of colorectal cancer. The Royal College of Pathologists, London. https://www.rcpath.org/profession/guidelines/cancer-datasets-and-tissue-pathways.html. Accessed 25 Sept 2018
Kakar S, Shi C, Berho ME, Driman DK, Fitzgibbons P, Frankel WL et al (2017) Protocol for the examination of specimens from patients with primary carcinoma of the colon and rectum. Arch Pathol Lab Med 133:1539–1551. https://doi.org/10.1043/1543-2165-133.10.1539
Ryan R, Gibbons D, Hyland JMP, 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
Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A (eds) (2010) AJCC cancer staging handbook, 7th edn. Springer, New-York
Sobin LH, Fleming ID (1997) TNM classification of malignant tumors, fifth edition. Cancer 80:1803–1804. https://doi.org/10.1002/(SICI)1097-0142(19971101)80:9<1803::AID-CNCR16>3.0.CO;2-9
Nederland VKG (2015) Richtlijn: Erfelijke darmkanker (2.0) https://www.mdl.nl/sites/www.mdl.nl/files/richlijnen/Erfelijke_darmkanker_-_december_2015_def.pdf. Accessed January 17, 2018
Chang GJ, Rodriguez-Bigas MA, Skibber JM, Moyer VA (2007) Lymph node evaluation and survival after curative resection of colon cancer: systematic review. J Natl Cancer Inst 99(6):433–441
Gavioli M, Luppi G, Losi L, Bertolini F, Santantonio M, Falchi AM, D’Amico R, Conte PF, Natalini G (2005) Incidence and clinical impact of sterilized disease and minimal residual disease after preoperative radiochemotherapy for rectal cancer. Dis Colon Rectum 48(10):1851–1857
Lim SB, Yu CS, Jang SJ, Kim TW, Kim JH, Kim JC (2010) Prognostic significance of lymphovascular invasion in sporadic colorectal cancer. Dis Colon Rectum 53(4):377–384
Labianca R, Nordlinger B, Beretta GD et al (2013) Early colon cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol 24:vi64–vi72. https://doi.org/10.1093/annonc/mdt354
Betge J, Pollheimer MJ, Lindtner RA, Kornprat P, Schlemmer A, Rehak P, Vieth M, Hoefler G, Langner C (2012) Intramural and extramural vascular invasion in colorectal cancer: prognostic significance and quality of pathology reporting. Cancer 118(3):628–638
Liebig C, Ayala G, Wilks J, Verstovsek G, Liu H, Agarwal N, Berger DH, Albo D (2009) Perineural invasion is an independent predictor of outcome in colorectal cancer. J Clin Oncol 27(31):5131–5137
Lugli A, Kirsch R, Ajioka Y, Bosman F, Cathomas G, Dawson H, el Zimaity H, Fléjou JF, Hansen TP, Hartmann A, Kakar S, Langner C, Nagtegaal I, Puppa G, Riddell R, Ristimäki A, Sheahan K, Smyrk T, Sugihara K, Terris B, Ueno H, Vieth M, Zlobec I, Quirke P (2017) Recommendations for reporting tumor budding in colorectal cancer based on the International Tumor Budding Consensus Conference (ITBCC) 2016. Mod Pathol 30:1299–1311. https://doi.org/10.1038/modpathol.2017.46
Bori R, Sejben I, Svébis M, Vajda K, Markó L, Pajkos G, Cserni G (2009) Heterogeneity of pT3 colorectal carcinomas according to the depth of invasion. Pathol Oncol Res 15(3):527–532 https://doi.org/10.1007/s12253-009-9149-x
Birbeck KF, Macklin CP, Tiffin NJ, Parsons W, Dixon MF, Mapstone NP, Abbott CR, Scott N, Finan PJ, Johnston D, Quirke P (2002) Rates of circumferential resection margin involvement vary between surgeons and predict outcomes in rectal cancer surgery. Ann Surg 235(4):449–457
Nagtegaal ID, Tot T, Jayne DG et al (2011) Lymph nodes, tumor deposits, and TNM: are we getting better? J Clin Oncol 29:2487–2492. https://doi.org/10.1200/JCO.2011.34.6429
Brierley JD, Gospodarowicz MK, Wittekind C (eds) (2016) International Union Against Cancer (UICC). TNM classification of malignant tumours, 8th edn. New York, Wiley-Blackwell
Amin MB, Edge SB, Greene FL et al (eds) (2017) American Joint Committee on Cancer (AJCC) cancer staging manual, 8th edn. New York, Springer
Molecular testing strategies for Lynch syndrome in people with colorectal syndrome in people with colorectal cancer (2017) https://www.nice.org.uk/guidance/dg27/resources/molecular-testing-strategies-for-lynch-syndrome-in-people-with-colorectal-cancer-pdf-1053695294917. Accessed December 8, 2017
Balmana J, Balaguer F, Cervantes A, Arnold D, ESMO Guidelines Working Group (2013) Familial risk-colorectal cancer: ESMO Clinical Practice Guidelines. Ann Oncol 24:vi73–vi80. https://doi.org/10.1093/annonc/mdt209
Umar A, Boland CR, Terdiman JP, Syngal S, Chapelle A, Ruschoff J, Fishel R, Lindor NM, Burgart LJ, Hamelin R, Hamilton SR, Hiatt RA, Jass J, Lindblom A, Lynch HT, Peltomaki P, Ramsey SD, Rodriguez-Bigas MA, Vasen HFA, Hawk ET, Barrett JC, Freedman AN, Srivastava S (2004) Revised Bethesda Guidelines for hereditary nonpolyposis colorectal cancer (Lynch syndrome) and microsatellite instability. J Natl Cancer Inst 96:261–268
Vasen HF, Watson P, Mecklin JP, Lynch HT (1999) New clinical criteria for hereditary nonpolyposis colorectal cancer (HNPCC, Lynch syndrome) proposed by the International Collaborative group on HNPCC. Gastroenterology 116:1453–1456
Van Cutsem E, Cervantes A, Adam R et al (2016) ESMO consensus guidelines for the management of patients with metastatic colorectal cancer. Ann Oncol 27:1386–1422. https://doi.org/10.1093/annonc/mdw235
RCPA (Royal College of Pathologists of Australasia) (2009) Guidelines for authors of structured cancer pathology reporting protocols. RCPA, Surry Hills
Palmer K, Nairn N, Guideline Development Group (2008) Management of acute gastrointestinal blood loss: summary of SIGN guidelines. BMJ 337:a1832
Appleton MA, Douglas-Jones AG, Morgan JM (1998) Evidence of effectiveness of clinical audit in improving histopathology reporting standards of mastectomy specimens. J Clin Pathol 51:30–33
Sluijter CE, van Lonkhuijzen LR, van Slooten NID, Overbeek LI (2016) The effects of implementing synoptic pathology reporting in cancer diagnosis: a systematic review. Virchows Arch 468(6):639–649. https://doi.org/10.1007/s00428-016-1935-8
Srigley JR, McGowan T, Maclean A, Raby M, Ross J, Kramer S, Sawka C (2009) Standardized synoptic cancer pathology reporting: a population-based approach. J Surg Oncol 99(8):517–524. https://doi.org/10.1002/jso.21282
International Collaboration on Cancer Reporting Guidelines for the Development of ICCR Datasets International Collaboration on Cancer Reporting (2016). http://www.iccr-cancer.org/ICCR/media/Documents/Guidelines-for-the-development-of-ICCR-datasets-2-6.pdf. Accessed January 16, 2018
Acknowledgements
The responders: Federica Grillo, Frank Carey, Snjezana Frkovic-Grazio, Camille Boulagnon-Rombi, Maurice Loughrey, Francois Paraf, Katerina Kamaradova, Peggy Dartigues, Bettina Rees, Timo Gaiser, Clare Fuller, Marie-Christine Saint-Paul, Rui Oliveira, Stefania Landolfi, Emyr Wyn Benbow, Billaud Elsa, Ricardo Fonseca, Anne Jouret-Mourin, Kevin West, Remi Picot, Eugene Mutijima, Cinzia Giacometti, Rob Goldin, Michael Taris, Yolanda Rodriguez-Gil, Ruth Düttmann, Nigel Scott, Marie-Danièle Diebold, Alejandro García-Varona, Dina Tiniakos, Luca Albarello, Flora Poizat, Marnix Jansen, Lígia Castro, Angus McGregor, Gorana Aralica, Branko Dmitrovic, Nevine El Deeb, Fulop Emoke, Caroline Gabignon, Paul Barrett, Norman Carr, Bruno Sinn, Sophie Michalak, Simona Gurzu, Giovanni De Petris, Danny Goudkade, Julia Rees, Isabelle Focke-Snieders, Michael Vieth, Adriana Martinez, Anne Couvelard, Antonella Savio, Desislava Tashkova, Caitlin Beggan, María-Luisa Sánchez-Bernal, Alessandro D’Amuri, Eugeniu Cazacu, Veena Shinde, Valeria Barresi, Kamran Ghaffarzadehgan, Jaroslaw Wejman,Ann Fleming, Maria-Jose Paules, Parag Dabir, Roberto Fiocca, Meleri Morgan, Olivia Cambero, Ioannis Provatas, Antonio Ieni, Ray McMahon, Catherine Julie, Roberto Salgado, Viorica Crisan, Izhar Bagwan, Gonca Ozgun, Bence Kővári, Carine De Prez, Adam Christian, Ana Cunha, Hajnalka Gyorffy, Andreea-Cristina Iogrescu, Marek Grega, Houria Belkralladi, Maria Brito, Leroux Agnès, Renata Chmelova, Florence Renaud, Felix Lasitschka, Nina Zidar, Karthik Kalyanasundaram, Armelle Bardier, Fiebo ten Kate, Jera Jeruc, Catherine lo Polito, Marie-Louise van Velthuysen, Nick West, Mukul Vij, Joost van Gorp, Vincenzo Villanacci, Frederic Bibeau, Ari Ristimäki, Nicholas Mapstone, Yasmine Lahoubi, Issam Abd-Alsmad, Xavier Sanjuan, Miriam Cuatrecasas, Carolina Ibarrola, Cecilia Egoavil Rojas, Eva Sticova, Fred Bosman, Manuela Vivario, Julian Ananiev, Maysa Al-Hussaini, Nathalie Guedj, Ana Dias, Christine Sempoux, Nicole van Grieken, Valentini Tzioufa-Asimakopoulou, Maria Gomez-Galdon, Maria Diodoro, Namor Williams, Kristina Tõnismäe, Calypso Barbatis,Fatima Carneiro, Elvira Gonzalez-Obeso, Gaetan MacGrogan, Isinsu Kuzu, Jens Neumann, Ratnadeep Ganguly, Daniel Val-Garijo, and those who did not submit their names. Technical support: Leonardo Perez-Aranda Alonso, Aida Molero-Bermejo, Vinciane Vincx, Katherine Hartmann, Jennifer Crespo, Francoise Meunier, Jouri Van Den Bergh, Jonathan O’Sullivan, Denis Lacombe, and Raed Al Dieri.
Contributions
Maria Urbanowicz, Heike I Grabsch, and Jean-François Fléjou conceived and designed the study and wrote, edited, and reviewed the manuscript. All authors researched and analyzed data and wrote, edited, and reviewed the manuscript and gave final approval for publication. All authors take full responsibility for the work as a whole, including the study design, access to data, and the decision to submit and publish the manuscript.
Funding
No funding was destined for this publication. Maria Urbanowicz’s work as Fellow at EORTC Headquarters was supported by a grant from the ESP and the EORTC Cancer Research Fund.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(DOCX 26 kb)
Rights and permissions
About this article
Cite this article
Urbanowicz, M., Grabsch, H.I., Fiteni, F. et al. An international survey-based study on colorectal cancer pathology reporting—guidelines versus local practice. Virchows Arch 473, 697–708 (2018). https://doi.org/10.1007/s00428-018-2457-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00428-018-2457-3