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Published in: Malaria Journal 1/2015

Open Access 01-12-2015 | Methodology

Bias in logistic regression due to imperfect diagnostic test results and practical correction approaches

Authors: Denis Valle, Joanna M. Tucker Lima, Justin Millar, Punam Amratia, Ubydul Haque

Published in: Malaria Journal | Issue 1/2015

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Abstract

Background

Logistic regression is a statistical model widely used in cross-sectional and cohort studies to identify and quantify the effects of potential disease risk factors. However, the impact of imperfect tests on adjusted odds ratios (and thus on the identification of risk factors) is under-appreciated. The purpose of this article is to draw attention to the problem associated with modelling imperfect diagnostic tests, and propose simple Bayesian models to adequately address this issue.

Methods

A systematic literature review was conducted to determine the proportion of malaria studies that appropriately accounted for false-negatives/false-positives in a logistic regression setting. Inference from the standard logistic regression was also compared with that from three proposed Bayesian models using simulations and malaria data from the western Brazilian Amazon.

Results

A systematic literature review suggests that malaria epidemiologists are largely unaware of the problem of using logistic regression to model imperfect diagnostic test results. Simulation results reveal that statistical inference can be substantially improved when using the proposed Bayesian models versus the standard logistic regression. Finally, analysis of original malaria data with one of the proposed Bayesian models reveals that microscopy sensitivity is strongly influenced by how long people have lived in the study region, and an important risk factor (i.e., participation in forest extractivism) is identified that would have been missed by standard logistic regression.

Conclusion

Given the numerous diagnostic methods employed by malaria researchers and the ubiquitous use of logistic regression to model the results of these diagnostic tests, this paper provides critical guidelines to improve data analysis practice in the presence of misclassification error. Easy-to-use code that can be readily adapted to WinBUGS is provided, enabling straightforward implementation of the proposed Bayesian models.
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Literature
1.
go back to reference Barbosa S, Gozze AB, Lima NF, Batista CL, Bastos MDS, Nicolete VC, et al. Epidemiology of disappearing Plasmodium vivax malaria: a case study in rural Amazonia. PLOS Negl Trop Dis. 2014;8:e3109.PubMedCentralCrossRefPubMed Barbosa S, Gozze AB, Lima NF, Batista CL, Bastos MDS, Nicolete VC, et al. Epidemiology of disappearing Plasmodium vivax malaria: a case study in rural Amazonia. PLOS Negl Trop Dis. 2014;8:e3109.PubMedCentralCrossRefPubMed
2.
go back to reference Acosta POA, Granja F, Meneses CA, Nascimento IAS, Sousa DD, Lima Junior WP, et al. False-negative dengue cases in Roraima, Brazil: an approach regarding the high number of negative results by NS1 AG kits. Rev Inst Med Trop Sao Paulo. 2014;56:447–50.PubMedCentralCrossRefPubMed Acosta POA, Granja F, Meneses CA, Nascimento IAS, Sousa DD, Lima Junior WP, et al. False-negative dengue cases in Roraima, Brazil: an approach regarding the high number of negative results by NS1 AG kits. Rev Inst Med Trop Sao Paulo. 2014;56:447–50.PubMedCentralCrossRefPubMed
3.
go back to reference Weigle KA, Labrada LA, Lozano C, Santrich C, Barker DC. PCR-based diagnosis of acute and chronic cutaneous leishmaniasis caused by Leishmania (Viannia). J Clin Microbiol. 2002;40:601–6.PubMedCentralCrossRefPubMed Weigle KA, Labrada LA, Lozano C, Santrich C, Barker DC. PCR-based diagnosis of acute and chronic cutaneous leishmaniasis caused by Leishmania (Viannia). J Clin Microbiol. 2002;40:601–6.PubMedCentralCrossRefPubMed
4.
go back to reference Baiden F, Webster J, Tivura M, Delimini R, Berko Y, Amenga-Etego S, et al. Accuracy of rapid tests for malaria and treatment outcomes for malaria and non-malaria cases among under-five children in rural Ghana. PLoS One. 2012;7:e34073.PubMedCentralCrossRefPubMed Baiden F, Webster J, Tivura M, Delimini R, Berko Y, Amenga-Etego S, et al. Accuracy of rapid tests for malaria and treatment outcomes for malaria and non-malaria cases among under-five children in rural Ghana. PLoS One. 2012;7:e34073.PubMedCentralCrossRefPubMed
5.
go back to reference Peeling RW, Artsob H, Pelegrino JL, Buchy P, Cardosa MJ, Devi S, et al. Evaluation of diagnostic tests: dengue. Nat Rev Microbiol. 2010;8:S30–8.CrossRefPubMed Peeling RW, Artsob H, Pelegrino JL, Buchy P, Cardosa MJ, Devi S, et al. Evaluation of diagnostic tests: dengue. Nat Rev Microbiol. 2010;8:S30–8.CrossRefPubMed
6.
go back to reference Amato Neto V, Amato VS, Tuon FF, Gakiya E, de Marchi CR, de Souza RM, et al. False-positive results of a rapid K39-based strip test and Chagas disease. Int J Infect Dis. 2009;13:182–5.CrossRefPubMed Amato Neto V, Amato VS, Tuon FF, Gakiya E, de Marchi CR, de Souza RM, et al. False-positive results of a rapid K39-based strip test and Chagas disease. Int J Infect Dis. 2009;13:182–5.CrossRefPubMed
7.
go back to reference Sundar S, Reed SG, Singh VP, Kumar PCK, Murray HW. Rapid accurate field diagnosis of Indian visceral leishmaniasis. Lancet. 1998;351:563–5.CrossRefPubMed Sundar S, Reed SG, Singh VP, Kumar PCK, Murray HW. Rapid accurate field diagnosis of Indian visceral leishmaniasis. Lancet. 1998;351:563–5.CrossRefPubMed
8.
go back to reference Mabey D, Peeling RW, Ustianowski A, Perkins MD. Diagnostics for the developing world. Nat Rev Microbiol. 2004;2:231–40.CrossRefPubMed Mabey D, Peeling RW, Ustianowski A, Perkins MD. Diagnostics for the developing world. Nat Rev Microbiol. 2004;2:231–40.CrossRefPubMed
9.
go back to reference Joseph L, Gyorkos TW, Coupal L. Bayesian estimation of disease prevalence and the parameters of diagnostic tests in the absence of a gold standard. Am J Epidemiol. 1995;141:263–72.PubMed Joseph L, Gyorkos TW, Coupal L. Bayesian estimation of disease prevalence and the parameters of diagnostic tests in the absence of a gold standard. Am J Epidemiol. 1995;141:263–72.PubMed
10.
go back to reference Speybroeck N, Praet N, Claes F, van Hong N, Torres K, Mao S, et al. True versus apparent malaria infection prevalence: the contribution of a Bayesian approach. PLoS One. 2011;6:e16705.PubMedCentralCrossRefPubMed Speybroeck N, Praet N, Claes F, van Hong N, Torres K, Mao S, et al. True versus apparent malaria infection prevalence: the contribution of a Bayesian approach. PLoS One. 2011;6:e16705.PubMedCentralCrossRefPubMed
11.
go back to reference Speybroeck N, Devleesschauwer B, Joseph L, Berkvens D. Misclassification errors in prevalence estimation: Bayesian handling with care. Int J Public Health. 2013;58:791–5.CrossRefPubMed Speybroeck N, Devleesschauwer B, Joseph L, Berkvens D. Misclassification errors in prevalence estimation: Bayesian handling with care. Int J Public Health. 2013;58:791–5.CrossRefPubMed
12.
go back to reference Neuhaus JM. Bias and efficiency loss due to misclassified responses in binary regression. Biometrika. 1999;86:843–55.CrossRef Neuhaus JM. Bias and efficiency loss due to misclassified responses in binary regression. Biometrika. 1999;86:843–55.CrossRef
13.
go back to reference Duffy SW, Warwick J, Williams ARW, Keshavarz H, Kaffashian F, Rohan TE, et al. A simple model for potential use with a misclassified binary outcome in epidemiology. J Epidemiol Commun Health. 2004;58:712–7.CrossRef Duffy SW, Warwick J, Williams ARW, Keshavarz H, Kaffashian F, Rohan TE, et al. A simple model for potential use with a misclassified binary outcome in epidemiology. J Epidemiol Commun Health. 2004;58:712–7.CrossRef
15.
go back to reference Magder LS, Hughes JP. Logistic regression when the outcome is measured with uncertainty. Am J Epidemiol. 1997;146:195–203.CrossRefPubMed Magder LS, Hughes JP. Logistic regression when the outcome is measured with uncertainty. Am J Epidemiol. 1997;146:195–203.CrossRefPubMed
16.
go back to reference Lyles RH, Tang L, Superak HM, King CC, Celentano DD, Lo Y, et al. Validation data-based adjustments for outcome misclassification in logistic regression: an illustration. Epidemiology. 2011;22:589–97.PubMedCentralCrossRefPubMed Lyles RH, Tang L, Superak HM, King CC, Celentano DD, Lo Y, et al. Validation data-based adjustments for outcome misclassification in logistic regression: an illustration. Epidemiology. 2011;22:589–97.PubMedCentralCrossRefPubMed
17.
go back to reference Fox MP, Lash TL, Greenland S. A method to automate probabilistic sensitivity analyses of misclassified binary variables. Int J Epidemiol. 2005;34:1370–6.CrossRefPubMed Fox MP, Lash TL, Greenland S. A method to automate probabilistic sensitivity analyses of misclassified binary variables. Int J Epidemiol. 2005;34:1370–6.CrossRefPubMed
18.
go back to reference McInturff P, Johnson WO, Cowling D, Gardner IA. Modelling risk when binary outcomes are subject to error. Stat Med. 2004;23:1095–109.CrossRefPubMed McInturff P, Johnson WO, Cowling D, Gardner IA. Modelling risk when binary outcomes are subject to error. Stat Med. 2004;23:1095–109.CrossRefPubMed
19.
go back to reference Valle D, Clark J. Improving the modeling of disease data from the government surveillance system: a case study on malaria in the Brazilian Amazon. PLoS Comput Biol. 2013;9:e1003312.PubMedCentralCrossRefPubMed Valle D, Clark J. Improving the modeling of disease data from the government surveillance system: a case study on malaria in the Brazilian Amazon. PLoS Comput Biol. 2013;9:e1003312.PubMedCentralCrossRefPubMed
20.
go back to reference Stamey JD, Young DM, Seaman JW Jr. A Bayesian approach to adjust for diagnostic misclassification between two mortality causes in Poisson regression. Stat Med. 2008;27:2440–52.CrossRefPubMed Stamey JD, Young DM, Seaman JW Jr. A Bayesian approach to adjust for diagnostic misclassification between two mortality causes in Poisson regression. Stat Med. 2008;27:2440–52.CrossRefPubMed
21.
go back to reference O’Meara WP, Barcus M, Wongsrichanalai C, Muth S, Maguire JD, Jordan RG, et al. Reader technique as a source of variability in determining malaria parasite density by microscopy. Malar J. 2006;5:118.PubMedCentralCrossRefPubMed O’Meara WP, Barcus M, Wongsrichanalai C, Muth S, Maguire JD, Jordan RG, et al. Reader technique as a source of variability in determining malaria parasite density by microscopy. Malar J. 2006;5:118.PubMedCentralCrossRefPubMed
22.
go back to reference Valle D, Clark J, Zhao K. Enhanced understanding of infectious diseases by fusing multiple datasets: a case study on malaria in the Western Brazilian Amazon region. PLoS One. 2011;6:e27462.PubMedCentralCrossRefPubMed Valle D, Clark J, Zhao K. Enhanced understanding of infectious diseases by fusing multiple datasets: a case study on malaria in the Western Brazilian Amazon region. PLoS One. 2011;6:e27462.PubMedCentralCrossRefPubMed
23.
go back to reference Silva-Nunes MD, Codeco CT, Malafronte RS, da Silva NS, Juncansen C, Muniz PT, et al. Malaria on the Amazonian frontier: transmission dynamics, risk factors, spatial distribution, and prospects for control. Am J Trop Med Hyg. 2008;79:624–35.PubMed Silva-Nunes MD, Codeco CT, Malafronte RS, da Silva NS, Juncansen C, Muniz PT, et al. Malaria on the Amazonian frontier: transmission dynamics, risk factors, spatial distribution, and prospects for control. Am J Trop Med Hyg. 2008;79:624–35.PubMed
24.
go back to reference Ladeia-Andrade S, Ferreira MU, de Carvalho ME, Curado I, Coura JR. Age-dependent acquisition of protective immunity to malaria in riverine populations of the Amazon Basin of Brazil. Am J Trop Med Hyg. 2009;80:452–9.PubMed Ladeia-Andrade S, Ferreira MU, de Carvalho ME, Curado I, Coura JR. Age-dependent acquisition of protective immunity to malaria in riverine populations of the Amazon Basin of Brazil. Am J Trop Med Hyg. 2009;80:452–9.PubMed
25.
go back to reference Alves FP, Durlacher RR, Menezes MJ, Krieger H, da Silva LHP, Camargo EP. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am J Trop Med Hyg. 2002;66:641–8.PubMed Alves FP, Durlacher RR, Menezes MJ, Krieger H, da Silva LHP, Camargo EP. High prevalence of asymptomatic Plasmodium vivax and Plasmodium falciparum infections in native Amazonian populations. Am J Trop Med Hyg. 2002;66:641–8.PubMed
26.
go back to reference Mtove G, Nadjm B, Amos B, Hendriksen ICE, Muro F, Reyburn H. Use of an HRP2-based rapid diagnostic test to guide treatment of children admitted to hospital in a malaria-endemic area of north-east Tanzania. Trop Med Int Health. 2011;16:545–50.PubMedCentralCrossRefPubMed Mtove G, Nadjm B, Amos B, Hendriksen ICE, Muro F, Reyburn H. Use of an HRP2-based rapid diagnostic test to guide treatment of children admitted to hospital in a malaria-endemic area of north-east Tanzania. Trop Med Int Health. 2011;16:545–50.PubMedCentralCrossRefPubMed
27.
go back to reference Onchiri FM, Pavlinac PB, Singa BO, Naulikha JM, Odundo EA, Farguhar C, et al. Frequency and correlates of malaria over-treatment in areas of differing malaria transmission: a cross-sectional study in rural Western Kenya. Malar J. 2015;14:97.PubMedCentralCrossRefPubMed Onchiri FM, Pavlinac PB, Singa BO, Naulikha JM, Odundo EA, Farguhar C, et al. Frequency and correlates of malaria over-treatment in areas of differing malaria transmission: a cross-sectional study in rural Western Kenya. Malar J. 2015;14:97.PubMedCentralCrossRefPubMed
28.
go back to reference van Genderen PJJ, van der Meer IM, Consten J, Petit PLC, van Gool T, Overbosch D. Evaluation of plasma lactate as a parameter for disease severity on admission in travelers with Plasmodium falciparum malaria. J Travel Med. 2005;12:261–4.CrossRefPubMed van Genderen PJJ, van der Meer IM, Consten J, Petit PLC, van Gool T, Overbosch D. Evaluation of plasma lactate as a parameter for disease severity on admission in travelers with Plasmodium falciparum malaria. J Travel Med. 2005;12:261–4.CrossRefPubMed
29.
go back to reference Alonzo TA, Pepe MS, Lumley T. Estimating disease prevalence in two-phase studies. Biostatistics. 2003;4:313–26.CrossRefPubMed Alonzo TA, Pepe MS, Lumley T. Estimating disease prevalence in two-phase studies. Biostatistics. 2003;4:313–26.CrossRefPubMed
30.
go back to reference Halloran ME, Longini IM Jr. Using validation sets for outcomes and exposure to infection in vaccine field studies. Am J Epidemiol. 2001;154:391–8.CrossRefPubMed Halloran ME, Longini IM Jr. Using validation sets for outcomes and exposure to infection in vaccine field studies. Am J Epidemiol. 2001;154:391–8.CrossRefPubMed
31.
go back to reference Black MA, Craig BA. Estimating disease prevalence in the absence of a gold standard. Stat Med. 2002;21:2653–69.CrossRefPubMed Black MA, Craig BA. Estimating disease prevalence in the absence of a gold standard. Stat Med. 2002;21:2653–69.CrossRefPubMed
32.
go back to reference Brenner H. Correcting for exposure misclassification using an alloyed gold standard. Epidemiology. 1996;7:406–10.CrossRefPubMed Brenner H. Correcting for exposure misclassification using an alloyed gold standard. Epidemiology. 1996;7:406–10.CrossRefPubMed
33.
go back to reference Tang L, Lyles RH, King CC, Celentano DD, Lo Y. Binary regression with differentially misclassified response and exposure variables. Stat Med. 2015;34:1605–20.CrossRefPubMed Tang L, Lyles RH, King CC, Celentano DD, Lo Y. Binary regression with differentially misclassified response and exposure variables. Stat Med. 2015;34:1605–20.CrossRefPubMed
34.
go back to reference Tang L, Lyles RH, King CC, Hogan JW, Lo Y. Regression analysis for differentially misclassified correlated binary outcomes. J R Stat Soc Ser C Appl Stat. 2015;64:433–49.CrossRefPubMed Tang L, Lyles RH, King CC, Hogan JW, Lo Y. Regression analysis for differentially misclassified correlated binary outcomes. J R Stat Soc Ser C Appl Stat. 2015;64:433–49.CrossRefPubMed
35.
go back to reference Richardson BB, Hughes JP. Product limit estimation for infectious disease data when the diagnostic test for the outcome is measured with uncertainty. Biostatistics. 2000;1:341–54.CrossRefPubMed Richardson BB, Hughes JP. Product limit estimation for infectious disease data when the diagnostic test for the outcome is measured with uncertainty. Biostatistics. 2000;1:341–54.CrossRefPubMed
Metadata
Title
Bias in logistic regression due to imperfect diagnostic test results and practical correction approaches
Authors
Denis Valle
Joanna M. Tucker Lima
Justin Millar
Punam Amratia
Ubydul Haque
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2015
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-015-0966-y

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