Skip to main content
Top
Published in: BMC Medical Research Methodology 1/2014

Open Access 01-12-2014 | Research article

Reducing decision errors in the paired comparison of the diagnostic accuracy of screening tests with Gaussian outcomes

Authors: Brandy M Ringham, Todd A Alonzo, John T Brinton, Sarah M Kreidler, Aarti Munjal, Keith E Muller, Deborah H Glueck

Published in: BMC Medical Research Methodology | Issue 1/2014

Login to get access

Abstract

Background

Scientists often use a paired comparison of the areas under the receiver operating characteristic curves to decide which continuous cancer screening test has the best diagnostic accuracy. In the paired design, all participants are screened with both tests. Participants with suspicious results or signs and symptoms of disease receive the reference standard test. The remaining participants are classified as non-cases, even though some may have occult disease. The standard analysis includes all study participants, which can create bias in the estimates of diagnostic accuracy since not all participants receive disease status verification. We propose a weighted maximum likelihood bias correction method to reduce decision errors.

Methods

Using Monte Carlo simulations, we assessed the method’s ability to reduce decision errors across a range of disease prevalences, correlations between screening test scores, rates of interval cases and proportions of participants who received the reference standard test.

Results

The performance of the method depends on characteristics of the screening tests and the disease and on the percentage of participants who receive the reference standard test. In studies with a large amount of bias in the difference in the full areas under the curves, the bias correction method reduces the Type I error rate and improves power for the correct decision. We demonstrate the method with an application to a hypothetical oral cancer screening study.

Conclusion

The bias correction method reduces decision errors for some paired screening trials. In order to determine if bias correction is needed for a specific screening trial, we recommend the investigator conduct a simulation study using our software.
Appendix
Available only for authorised users
Literature
1.
go back to reference Lingen MW: Efficacy of oral cancer screening adjunctive techniques. National Institute of Dental and Craniofacial Research, National Institutes of Health, US Department of Health and Human Services. NIH Project Number 1RC2DE020779-01. 2009, Lingen MW: Efficacy of oral cancer screening adjunctive techniques. National Institute of Dental and Craniofacial Research, National Institutes of Health, US Department of Health and Human Services. NIH Project Number 1RC2DE020779-01. 2009,
2.
go back to reference Lewin JM, D’Orsi CJ, Hendrick RE, Moss LJ, Isaacs PK, Karellas A, Cutter GR: Clinical comparison of full-field digital mammography and screen-film mammography for detection of breast cancer. Am J Roentgenol. 2002, 179: 671-677. 10.2214/ajr.179.3.1790671.CrossRef Lewin JM, D’Orsi CJ, Hendrick RE, Moss LJ, Isaacs PK, Karellas A, Cutter GR: Clinical comparison of full-field digital mammography and screen-film mammography for detection of breast cancer. Am J Roentgenol. 2002, 179: 671-677. 10.2214/ajr.179.3.1790671.CrossRef
3.
go back to reference Pisano ED, Gatsonis C, Hendrick E, Yaffe M, Baum JK, Acharyya S, Conant EF, Fajardo LL, Bassett L, D’Orsi C, Jong R, Rebner M: Diagnostic performance of digital versus film mammography for breast-cancer screening. N Engl J Med. 2005, 253: 1773-1783.CrossRef Pisano ED, Gatsonis C, Hendrick E, Yaffe M, Baum JK, Acharyya S, Conant EF, Fajardo LL, Bassett L, D’Orsi C, Jong R, Rebner M: Diagnostic performance of digital versus film mammography for breast-cancer screening. N Engl J Med. 2005, 253: 1773-1783.CrossRef
4.
go back to reference Glueck DH, Lamb MM, O’Donnell CI, Ringham BM, Brinton JT, Muller KE, Lewin JM: Bias in trials comparing paired continuous tests can cause researchers to choose the wrong screening modality. BMC Med Res Methodol. 2009, 9: 4-10.1186/1471-2288-9-4.CrossRefPubMedPubMedCentral Glueck DH, Lamb MM, O’Donnell CI, Ringham BM, Brinton JT, Muller KE, Lewin JM: Bias in trials comparing paired continuous tests can cause researchers to choose the wrong screening modality. BMC Med Res Methodol. 2009, 9: 4-10.1186/1471-2288-9-4.CrossRefPubMedPubMedCentral
5.
go back to reference Lijmer JG, Mol BW, Heisterkamp S, Bonsel GJ, Prins MH, van der Meulen JH, Bossuyt PM: Empirical evidence of design-related bias in studies of diagnostic tests. JAMA. 1999, 282: 1061-1066. 10.1001/jama.282.11.1061.CrossRefPubMed Lijmer JG, Mol BW, Heisterkamp S, Bonsel GJ, Prins MH, van der Meulen JH, Bossuyt PM: Empirical evidence of design-related bias in studies of diagnostic tests. JAMA. 1999, 282: 1061-1066. 10.1001/jama.282.11.1061.CrossRefPubMed
6.
go back to reference Reitsma JB, Rutjes AWS, Khan KS, Coomarasamy A, Bossuyt PM: A review of solutions for diagnostic accuracy studies with an imperfect or missing reference standard. J Clin Epidemiol. 2009, 62: 797-806. 10.1016/j.jclinepi.2009.02.005.CrossRefPubMed Reitsma JB, Rutjes AWS, Khan KS, Coomarasamy A, Bossuyt PM: A review of solutions for diagnostic accuracy studies with an imperfect or missing reference standard. J Clin Epidemiol. 2009, 62: 797-806. 10.1016/j.jclinepi.2009.02.005.CrossRefPubMed
7.
go back to reference Rutjes AWS, Reitsma JB, Di Nisio, Smidt N, van Rijn, Bossuyt PMM: Evidence of bias and variation in diagnostic accuracy studies. Can Med Assoc J. 2006, 174: 469-476. 10.1503/cmaj.050090.CrossRef Rutjes AWS, Reitsma JB, Di Nisio, Smidt N, van Rijn, Bossuyt PMM: Evidence of bias and variation in diagnostic accuracy studies. Can Med Assoc J. 2006, 174: 469-476. 10.1503/cmaj.050090.CrossRef
8.
go back to reference Whiting P, Rutjes AWS, Reitsma JB, Glas AS, Bossuyt PMM, Kleijnen J: Sources of variation and bias in studies of diagnostic accuracy: a systematic review. Ann Intern Med. 2004, 140: 189-202. 10.7326/0003-4819-140-3-200402030-00010.CrossRefPubMed Whiting P, Rutjes AWS, Reitsma JB, Glas AS, Bossuyt PMM, Kleijnen J: Sources of variation and bias in studies of diagnostic accuracy: a systematic review. Ann Intern Med. 2004, 140: 189-202. 10.7326/0003-4819-140-3-200402030-00010.CrossRefPubMed
9.
go back to reference Ringham BM, Alonzo TA, Grunwald GK, Glueck DH: Estimates of sensitivity and specificity can be biased when reporting the results of the second test in a screening trial conducted in series. BMC Med Res Methodol. 2010, 10: 3-10.1186/1471-2288-10-3.CrossRefPubMedPubMedCentral Ringham BM, Alonzo TA, Grunwald GK, Glueck DH: Estimates of sensitivity and specificity can be biased when reporting the results of the second test in a screening trial conducted in series. BMC Med Res Methodol. 2010, 10: 3-10.1186/1471-2288-10-3.CrossRefPubMedPubMedCentral
10.
go back to reference Kish L: Survey Sampling. 1965, Hoboken: John Wiley & Sons, Kish L: Survey Sampling. 1965, Hoboken: John Wiley & Sons,
11.
go back to reference Nath GB: Estimation in truncated bivariate normal distributions. J Roy Stat Soc C-App. 1971, 20: 313-319. Nath GB: Estimation in truncated bivariate normal distributions. J Roy Stat Soc C-App. 1971, 20: 313-319.
12.
go back to reference Ross S: A First Course in Probability. 2009, Prentice Hall: Upper Saddle River, Ross S: A First Course in Probability. 2009, Prentice Hall: Upper Saddle River,
14.
go back to reference Metz CE, Herman BA, Shen JH: Maximum likelihood estimation of receiver operating characteristic (roc) curves from continuously-distributed data. Stat Med. 1998, 17: 1033-1053. 10.1002/(SICI)1097-0258(19980515)17:9<1033::AID-SIM784>3.0.CO;2-Z.CrossRefPubMed Metz CE, Herman BA, Shen JH: Maximum likelihood estimation of receiver operating characteristic (roc) curves from continuously-distributed data. Stat Med. 1998, 17: 1033-1053. 10.1002/(SICI)1097-0258(19980515)17:9<1033::AID-SIM784>3.0.CO;2-Z.CrossRefPubMed
15.
go back to reference Obuchowski NA, McClish DK: Sample size determination for diagnostic accuracy studies involving binormal roc curve indices. Stat Med. 1997, 16: 1529-1542. 10.1002/(SICI)1097-0258(19970715)16:13<1529::AID-SIM565>3.0.CO;2-H.CrossRefPubMed Obuchowski NA, McClish DK: Sample size determination for diagnostic accuracy studies involving binormal roc curve indices. Stat Med. 1997, 16: 1529-1542. 10.1002/(SICI)1097-0258(19970715)16:13<1529::AID-SIM565>3.0.CO;2-H.CrossRefPubMed
16.
go back to reference Bunker CH, Patrick AL, Konety BR, Dhir R, Brufsky AM, Vivas CA, Becich MJ, Trump DL, Kuller LH: High prevalence of screening-detected prostate cancer among afro-caribbeans: the tobago prostate cancer survey. Cancer Epidem Biomar. 2002, 11: 726-729. Bunker CH, Patrick AL, Konety BR, Dhir R, Brufsky AM, Vivas CA, Becich MJ, Trump DL, Kuller LH: High prevalence of screening-detected prostate cancer among afro-caribbeans: the tobago prostate cancer survey. Cancer Epidem Biomar. 2002, 11: 726-729.
17.
go back to reference Lim K, Moles DR, Downer MC, Speight PM: Opportunistic screening for oral cancer and precancer in general dental practice: results of a demonstration study. Brit Dent J. 2003, 194: 497-502. 10.1038/sj.bdj.4810069.CrossRefPubMed Lim K, Moles DR, Downer MC, Speight PM: Opportunistic screening for oral cancer and precancer in general dental practice: results of a demonstration study. Brit Dent J. 2003, 194: 497-502. 10.1038/sj.bdj.4810069.CrossRefPubMed
19.
go back to reference Bobo JK, Lee NC, Thames SF: Findings from 752,081 clinical breast examinations reported to a national screening program from 1995 through 1998. J Natl Cancer I. 2000, 92: 971-976. 10.1093/jnci/92.12.971.CrossRef Bobo JK, Lee NC, Thames SF: Findings from 752,081 clinical breast examinations reported to a national screening program from 1995 through 1998. J Natl Cancer I. 2000, 92: 971-976. 10.1093/jnci/92.12.971.CrossRef
20.
go back to reference Alonzo TA: Verification bias-corrected estimators of the relative true and false positive rates of two binary screening tests. Stat Med. 2005, 24: 403-417. 10.1002/sim.1959.CrossRefPubMed Alonzo TA: Verification bias-corrected estimators of the relative true and false positive rates of two binary screening tests. Stat Med. 2005, 24: 403-417. 10.1002/sim.1959.CrossRefPubMed
22.
go back to reference Begg CB, Greenes RA: Assessment of diagnostic tests when disease verification is subject to selection bias. Biometrics. 1983, 39: 207-215. 10.2307/2530820.CrossRefPubMed Begg CB, Greenes RA: Assessment of diagnostic tests when disease verification is subject to selection bias. Biometrics. 1983, 39: 207-215. 10.2307/2530820.CrossRefPubMed
23.
go back to reference Alonzo TA, Pepe MS: Assessing accuracy of a continuous screening test in the presence of verification bias. J Roy Stat Soc C-App. 2005, 54: 173-190. 10.1111/j.1467-9876.2005.00477.x.CrossRef Alonzo TA, Pepe MS: Assessing accuracy of a continuous screening test in the presence of verification bias. J Roy Stat Soc C-App. 2005, 54: 173-190. 10.1111/j.1467-9876.2005.00477.x.CrossRef
24.
go back to reference Buzoianu M, Kadane JB: Adjusting for verification bias in diagnostic test evaluation: A bayesian approach. Stat Med. 2008, 27: 2453-2473. 10.1002/sim.3099.CrossRefPubMed Buzoianu M, Kadane JB: Adjusting for verification bias in diagnostic test evaluation: A bayesian approach. Stat Med. 2008, 27: 2453-2473. 10.1002/sim.3099.CrossRefPubMed
25.
go back to reference Martinez EZ, Alberto Achcar, Louzada-Neto F: Estimators of sensitivity and specificity in the presence of verification bias: a bayesian approach. Comput Stat Data An. 2006, 51: 601-611. 10.1016/j.csda.2005.12.021.CrossRef Martinez EZ, Alberto Achcar, Louzada-Neto F: Estimators of sensitivity and specificity in the presence of verification bias: a bayesian approach. Comput Stat Data An. 2006, 51: 601-611. 10.1016/j.csda.2005.12.021.CrossRef
26.
go back to reference Rotnitzky A, Faraggi D, Schisterman E: Doubly robust estimation of the area under the receiver-operating characteristic curve in the presence of verification bias. J Am Stat Assoc. 2006, 101: 1276-1288. 10.1198/016214505000001339.CrossRef Rotnitzky A, Faraggi D, Schisterman E: Doubly robust estimation of the area under the receiver-operating characteristic curve in the presence of verification bias. J Am Stat Assoc. 2006, 101: 1276-1288. 10.1198/016214505000001339.CrossRef
27.
go back to reference Toledano AY, Gatsonis C: Generalized estimating equations for ordinal categorical data: arbitrary patterns of missing responses and missingness in a key covariate. Biometrics. 1999, 55: 488-496. 10.1111/j.0006-341X.1999.00488.x.CrossRefPubMed Toledano AY, Gatsonis C: Generalized estimating equations for ordinal categorical data: arbitrary patterns of missing responses and missingness in a key covariate. Biometrics. 1999, 55: 488-496. 10.1111/j.0006-341X.1999.00488.x.CrossRefPubMed
28.
go back to reference Zhou X: Maximum likelihood estimators of sensitivity and specificity corrected for verification bias. Commun Stat A-Theor. 1993, 22: 3177-3198. 10.1080/03610929308831209.CrossRef Zhou X: Maximum likelihood estimators of sensitivity and specificity corrected for verification bias. Commun Stat A-Theor. 1993, 22: 3177-3198. 10.1080/03610929308831209.CrossRef
29.
go back to reference Vacek PM: The effect of conditional dependence on the evaluation of diagnostic tests. Biometrics. 1985, 41: 959-968. 10.2307/2530967.CrossRefPubMed Vacek PM: The effect of conditional dependence on the evaluation of diagnostic tests. Biometrics. 1985, 41: 959-968. 10.2307/2530967.CrossRefPubMed
30.
go back to reference Torrance-Rynard VL, Walter SD: Effects of dependent errors in the assessment of diagnostic test performance. Stat Med. 1997, 16: 2157-2175. 10.1002/(SICI)1097-0258(19971015)16:19<2157::AID-SIM653>3.0.CO;2-X.CrossRefPubMed Torrance-Rynard VL, Walter SD: Effects of dependent errors in the assessment of diagnostic test performance. Stat Med. 1997, 16: 2157-2175. 10.1002/(SICI)1097-0258(19971015)16:19<2157::AID-SIM653>3.0.CO;2-X.CrossRefPubMed
31.
go back to reference Metz C, Kronman HA, Wang P: New approach for testing the significance of differences between roc curves measured from correlated data. Information Processing In Medical Imaging. Edited by: Deconinck F. 1984, The Hague: Springer, 432-445.CrossRef Metz C, Kronman HA, Wang P: New approach for testing the significance of differences between roc curves measured from correlated data. Information Processing In Medical Imaging. Edited by: Deconinck F. 1984, The Hague: Springer, 432-445.CrossRef
32.
go back to reference Elashoff D, Zhou H, Reiss J, Wang J, Xiao H, Henson B, Hu S, Arellano M, Sinha U, Le A, Messadi D, Wang M, Nabili V, Lingen M, Morris D, Randolph T, Feng Z, Akin D, Kastratovic DA, Chia D, Abemayor E, Wong DTW: Prevalidation of salivary biomarkers for oral cancer detection. Cancer Epidem Biomar. 2012, 21: 664-672. 10.1158/1055-9965.EPI-11-1093.CrossRef Elashoff D, Zhou H, Reiss J, Wang J, Xiao H, Henson B, Hu S, Arellano M, Sinha U, Le A, Messadi D, Wang M, Nabili V, Lingen M, Morris D, Randolph T, Feng Z, Akin D, Kastratovic DA, Chia D, Abemayor E, Wong DTW: Prevalidation of salivary biomarkers for oral cancer detection. Cancer Epidem Biomar. 2012, 21: 664-672. 10.1158/1055-9965.EPI-11-1093.CrossRef
Metadata
Title
Reducing decision errors in the paired comparison of the diagnostic accuracy of screening tests with Gaussian outcomes
Authors
Brandy M Ringham
Todd A Alonzo
John T Brinton
Sarah M Kreidler
Aarti Munjal
Keith E Muller
Deborah H Glueck
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Medical Research Methodology / Issue 1/2014
Electronic ISSN: 1471-2288
DOI
https://doi.org/10.1186/1471-2288-14-37

Other articles of this Issue 1/2014

BMC Medical Research Methodology 1/2014 Go to the issue