Abstract
Background
Faecal samples collected and stored frozen over years may be a valuable resource for efficient retrospective evaluation of faecal immunochemical tests (FITs). We aimed to assess how prolonged frozen storage and freeze-thaw cycles might affect measures of faecal haemoglobin (Hb) and diagnostic performance of FITs.
Methods
From 2005 through 2010, participants of screening colonoscopy (n = 2042) and clinical colorectal cancer (CRC) cases (n = 184) provided faecal samples in stool containers (60 mL). The samples were stored at −80 °C for up to 11 years and underwent three freeze-thaw cycles. Between each cycle, a defined amount of faeces was extracted using the manufacturer’s sampling device of one or two FITs (RIDASCREEN, OC-Sensor). Faecal Hb concentration and diagnostic performance were calculated and compared across freeze-thaw cycles.
Results
For RIDASCREEN and the OC-Sensor, repeat measurements were available for 504 and 551 study participants, respectively. Hb concentrations correlated strongly (0.77 and 0.85, respectively) and diagnostic performance indicators were similar at the repeat measurements among the same FITs. For RIDASCREEN we found even slightly higher Hb levels, sensitivities and area under the curves (AUCs) after the third than after the first freeze-thaw cycle. For the OC-Sensor the Hb levels, sensitivities and AUCs were slightly lower after prolonged storage and one additional freeze-thaw cycle.
Conclusions
Measures of Hb and diagnostic performance were fairly stable, even after long-term frozen storage and multiple freeze-thaw cycles of raw faecal samples. Faecal samples collected in prospective screening studies and kept frozen at −80 °C before analysis seem useful for timely and efficient retrospective evaluation of FIT performance.
Acknowledgments
The authors thank Dr. Katarina Cuk for her help in conducting the project. They also thank Sabine Eichenherr, Romana Kimmel and Ulrike Schlesselmann for their excellent work in laboratory preparation of stool samples, and Volker Herrmann for his help in preparing the project.
Author contributions: AG coordinated the project and contributed to the fieldwork and laboratory analyses, carried out the statistical analyses and drafted the manuscript. TN, KW, PSK and MH contributed to revision of the manuscript for important intellectual content. HB designed, led and supervised the study and contributed to revision of the manuscript for important intellectual content. All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Disclosures: The authors disclose no conflicts of interest. All test kits were provided free of charge by the manufacturers. The manufacturers had no role in the study design, in the collection, analysis, and interpretation of data, or approval of submission for presentation/publication.
References
1. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68:394–424.10.3322/caac.21492Search in Google Scholar PubMed
2. von Karsa L, Patnick J, Segnan N, Atkin W, Halloran S, Lansdorp-Vogelaar I, et al. European guidelines for quality assurance in colorectal cancer screening and diagnosis: overview and introduction to the full supplement publication. Endoscopy 2013;45:51–9.10.1055/s-0032-1325997Search in Google Scholar
3. Sung JJ, Ng SC, Chan FK, Chiu HM, Kim HS, Matsuda T, et al. An updated Asia Pacific Consensus Recommendations on colorectal cancer screening. Gut 2015;64:121–32.10.1136/gutjnl-2013-306503Search in Google Scholar PubMed
4. Bibbins-Domingo K, Grossman DC, Curry SJ, Davidson KW, Epling Jr. JW, Garcia FA, et al. Screening for colorectal cancer: US Preventive Services Task Force Recommendation Statement. J Am Med Assoc 2016;315:2564–75.10.1001/jama.2016.5989Search in Google Scholar PubMed
5. Schreuders EH, Ruco A, Rabeneck L, Schoen RE, Sung JJ, Young GP, et al. Colorectal cancer screening: a global overview of existing programmes. Gut 2015;64:1637–49.10.1136/gutjnl-2014-309086Search in Google Scholar PubMed
6. Gies A, Bhardwaj M, Stock C, Schrotz-King P, Brenner H. Quantitative fecal immunochemical tests for colorectal cancer screening. Int J Cancer 2018;143:234–44.10.1002/ijc.31233Search in Google Scholar PubMed
7. Gies A, Cuk K, Schrotz-King P, Brenner H. Direct comparison of diagnostic performance of 9 quantitative fecal immunochemical tests for colorectal cancer screening. Gastroenterology 2018;154:93–104.10.1053/j.gastro.2017.09.018Search in Google Scholar PubMed
8. Bossuyt PM, Reitsma JB, Bruns DE, Gatsonis CA, Glasziou PP, Irwig L, et al. STARD 2015: an updated list of essential items for reporting diagnostic accuracy studies. Br Med J 2015;351:h5527.10.1136/bmj.h5527Search in Google Scholar PubMed PubMed Central
9. Fraser CG, Allison JE, Young GP, Halloran SP, Seaman HE. Improving the reporting of evaluations of faecal immunochemical tests for haemoglobin: the FITTER standard and checklist. Eur J Cancer Prev 2015;24:24–6.10.1097/CEJ.0000000000000016Search in Google Scholar PubMed
10. Hundt S, Haug U, Brenner H. Comparative evaluation of immunochemical fecal occult blood tests for colorectal adenoma detection. Ann Intern Med 2009;150:162–9.10.7326/0003-4819-150-3-200902030-00005Search in Google Scholar PubMed
11. Brenner H, Tao S, Haug U. Low-dose aspirin use and performance of immunochemical fecal occult blood tests. J Am Med Assoc 2010;304:2513–20.10.1001/jama.2010.1773Search in Google Scholar PubMed
12. Brenner H, Tao S. Superior diagnostic performance of faecal immunochemical tests for haemoglobin in a head-to-head comparison with guaiac based faecal occult blood test among 2235 participants of screening colonoscopy. Eur J Cancer 2013;49:3049–54.10.1016/j.ejca.2013.04.023Search in Google Scholar PubMed
13. Tao S, Seiler CM, Ronellenfitsch U, Brenner H. Comparative evaluation of nine faecal immunochemical tests for the detection of colorectal cancer. Acta Oncol 2013;52:1667–75.10.3109/0284186X.2013.789141Search in Google Scholar PubMed
14. Fraser CG, Allison JE, Halloran SP, Young GP, on behalf of the Expert Working Group on Fecal Immunochemical Tests for Hemoglobin Colorectal Cancer Screening Committee, World Endoscopy Organization. A proposal to standardize reporting units for fecal immunochemical tests for hemoglobin. J Natl Cancer Inst 2012;104:810–4.10.1093/jnci/djs190Search in Google Scholar PubMed
15. DeLong ER, DeLong DM, Clarke-Pearson DL. Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 1988;44:837–45.10.2307/2531595Search in Google Scholar
16. Burton RM, Landreth KS, Barrows GH, Jarrett DD, Songster CL. Appearance, properties, and origin of altered human hemoglobin in feces. Lab Invest 1976;35:111–5.Search in Google Scholar
17. Rose IS, Young GP, St John DJ, Deacon MC, Blake D, Henderson RW. Effect of ingestion of hemoproteins on fecal excretion of hemes and porphyrins. Clin Chem 1989;35:2290–6.10.1093/clinchem/35.12.2290Search in Google Scholar
18. Young GP, Symonds EL, Allison JE, Cole SR, Fraser CG, Halloran SP, et al. Advances in fecal occult blood tests: the FIT revolution. Dig Dis Sci 2015;60:609–22.10.1007/s10620-014-3445-3Search in Google Scholar PubMed PubMed Central
19. Grazzini G, Ventura L, Zappa M, Ciatto S, Confortini M, Rapi S, et al. Influence of seasonal variations in ambient temperatures on performance of immunochemical faecal occult blood test for colorectal cancer screening: observational study from the Florence district. Gut 2010;59:1511–5.10.1136/gut.2009.200873Search in Google Scholar PubMed
20. van Roon AH, Hol L, van Vuuren AJ, Francke J, Ouwendijk M, Heijens A, et al. Are fecal immunochemical test characteristics influenced by sample return time? A population-based colorectal cancer screening trial. Am J Gastroenterol 2012;107:99–107.10.1038/ajg.2011.396Search in Google Scholar PubMed
21. Symonds EL, Osborne JM, Cole SR, Bampton PA, Fraser RJ, Young GP. Factors affecting faecal immunochemical test positive rates: demographic, pathological, behavioural and environmental variables. J Med Screen 2015;22:187–93.10.1177/0969141315584783Search in Google Scholar PubMed
22. Doubeni CA, Jensen CD, Fedewa SA, Quinn VP, Zauber AG, Schottinger JE, et al. Fecal immunochemical test (FIT) for colon cancer screening: variable performance with ambient temperature. J Am Board Fam Med 2016;29:672–81.10.3122/jabfm.2016.06.160060Search in Google Scholar PubMed PubMed Central
23. van Rossum LG, van Rijn AF, van Oijen MG, Fockens P, Laheij RJ, Verbeek AL, et al. False negative fecal occult blood tests due to delayed sample return in colorectal cancer screening. Int J Cancer 2009;125:746–50.10.1002/ijc.24458Search in Google Scholar PubMed
24. Niedermaier T, Weigl K, Gies A, Hoffmeister M, Brenner H. Accuracy of a fecal immunochemical test according to outside temperature and travel time. Clin Epidemiol 2018;10:1203–13.10.2147/CLEP.S170169Search in Google Scholar PubMed PubMed Central
25. Gies A, Cuk K, Schrotz-King P, Brenner H. Direct comparison of ten quantitative fecal immunochemical tests for hemoglobin stability in colorectal cancer screening. Clin Transl Gastroenterol 2018;9:168.10.1038/s41424-018-0035-2Search in Google Scholar PubMed PubMed Central
26. Symonds EL, Cole SR, Bastin D, Fraser RJ, Young GP. Effect of sample storage temperature and buffer formulation on faecal immunochemical test haemoglobin measurements. J Med Screen 2017;24:176–81.10.1177/0969141316686808Search in Google Scholar PubMed
27. Catomeris P, Baxter NN, Boss SC, Paszat LF, Rabeneck L, Randell E, et al. Effect of temperature and time on fecal hemoglobin stability in 5 fecal immunochemical test methods and one guaiac method. Arch Pathol Lab Med 2018;142:75–82.10.5858/arpa.2016-0294-OASearch in Google Scholar PubMed
28. Chen H, Werner S, Brenner H. Fresh vs frozen samples and ambient temperature have little effect on detection of colorectal cancer or adenomas by a fecal immunochemical test in a colorectal cancer screening cohort in Germany. Clin Gastroenterol Hepatol 2017;15:1547–56.e5.10.1016/j.cgh.2016.10.018Search in Google Scholar PubMed
©2020 Walter de Gruyter GmbH, Berlin/Boston
