Data Science; Epidemiology; Modelling; Plant Science; Agronomy and Crop Science
Abstract :
[en] Disease severity in plant pathology is often measured by the amount of a plant or plant part that exhibits disease symptoms. This is typically assessed using a numerical scale, which allows for a standardized, convenient, and quick method of rating. These scales, known as "quantitative ordinal scales" (QOS), divide the percentage scale into a predetermined number of intervals. There are various ways to analyze this ordinal data, with traditional methods involving the use of mid-point conversion to represent the interval. However, this may not be precise enough, as it is only an estimate of the true value. In this case, the data may be considered "interval-censored," meaning that we have some knowledge of the value but not an exact measurement. This type of uncertainty is known as "censoring" and techniques that address censoring, such as survival analysis (SA), use all available information and account for this uncertainty. To investigate the pros and cons of using SA with QOS measurements, we conducted a simulation based on three pathosystems. The results showed that SA almost always outperformed the mid-point conversion with data analyzed using a t-test, particularly when data was not normally distributed. The mid-point conversion is currently a standard procedure. In certain cases, the mid-point approach required a 400% increase in sample size in order to achieve the same power as the SA method. We conclude that SA is a valuable method for enhancing the power of hypothesis testing when analyzing QOS severity data.
Disciplines :
Agriculture & agronomy
Author, co-author :
Chiang, Kuo-Szu; National Chung Hsing University, Agronomy, 250, Kuo Kuang Road, Taichung, Taiwan, 402, kucst@dragon.nchu.edu.tw
Chang, Y M; Taichung, Taiwan, yumei0115@thu.edu.tw
Liu, H I; New Taipei City, Taiwan, oeliu@mail.mcut.edu.tw
Lee, J Y; Taichung, Taiwan, jylee@fcu.edu.tw
El Jarroudi, Moussa ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement (Arlon Campus Environnement) > Eau, Environnement, Développement
Bock, Clive; Byron, United States, clive.bock@ars.usda.gov
Language :
English
Title :
Survival Analysis as a Basis to Test Hypotheses When Using Quantitative Ordinal Scale Disease Severity Data.
Alisaac, E., Behmann, J., Kuska, M. T., Dehne, H.-W., and Mahlein, A.-K. 2018. Hyperspectral quantification of wheat resistance to Fusarium head blight: Comparison of two Fusarium species. Eur. J. Plant Pathol. 152:869-884.
American Phytopathological Society. 2022. Information for Authors. American Phytopathological Society, St. Paul, MN. http://apsjournals.apsnet.org/page/ authorinformation#geninfo
Bock, C. H., Barbedo, J. G. A., Del Ponte, E. M., Bohnenkamp, D., and Mahlein, A.-K. 2020. From visual estimates to fully automated sensor-based measurements of plant disease severity: Status and challenges for improving accuracy. Phytopathol. Res. 2:9.
Bock, C. H., Chiang, K.-S., and Del Ponte, E. M. 2022a. Plant disease severity estimated visually: A century of research, best practices and opportunities for improving methods and practices to maximize accuracy. Trop. Plant Pathol. 47:25-42.
Bock, C. H., El Jarroudi, M., Kouadio, A. L., Mackels, C., Chiang, K.-S., and Delfosse, P. 2015. Disease severity estimates—Effects of rater accuracy and assessment methods for comparing treatments. Plant Dis. 99:1104-1112.
Bock, C. H., Gottwald, T. R., Parker, P. E., Ferrandino, F., Welham, S., van den Bosch, F., and Parnell, S. 2010a. Some consequences of using the Horsfall–Barratt scale for hypothesis testing. Phytopathology 100:1030-1041.
Bock, C. H., Parker, P. E., Cook, A. Z., and Gottwald, T. R. 2008a. Visual rating and the use of image analysis for assessing different symptoms of citrus canker on grapefruit leaves. Plant Dis. 92:530-541.
Bock, C. H., Parker, P. E., Cook, A. Z., and Gottwald, T. R. 2008b. Characteristics of the perception of different severity measures of citrus canker and the relationships between the various symptom types. Plant Dis. 92: 927-939.
Bock, C. H., Parker, P. E., Cook, A. Z., Riley, T., and Gottwald, T. R. 2009. Comparison of assessment of citrus canker foliar symptoms by experienced and inexperienced raters. Plant Dis. 93:412-424.
Bock, C. H., Pethybridge, S. J., Barbedo, J. G. A., Esker, P. D., Mahlein, A.-K., and Del Ponte, E. M. 2022b. A phytopathometry glossary for the twenty-first century: Towards consistency and precision in intra- and inter-disciplinary dialogues. Trop. Plant Pathol. 47:14-24.
Bock, C. H., Poole, G. H., Parker, P. E., and Gottwald, T. R. 2010b. Plant disease severity estimated visually, by digital photography and image analysis, and by hyperspectral imaging. Crit. Rev. Plant Sci. 29:59-107.
Bock, C. H., Wood, B. W., van den Bosch, F., Parnell, S., and Gottwald, T. R. 2013. The effect of Horsfall–Barratt category size on the accuracy and reliability of estimates of pecan scab severity. Plant Dis. 97:797-806.
Bogaerts, K., Komárek, A., and Lesaffre, E. 2018. Survival Analysis with Interval-Censored Data: A Practical Approach with Examples in R, SAS, and BUGS. Chapman & Hall/CRC, Boca Raton, FL.
Chen, M., Brun, F., Raynal, M., and Makowski, D. 2019. Timing of grape downy mildew onset in Bordeaux vineyards. Phytopathology 109:787-795.
Chiang, K.-S., and Bock, C. H. 2022. Understanding the ramifications of quantitative ordinal scales on accuracy of estimates of disease severity and data analysis in plant pathology. Trop. Plant Pathol. 47:58-73.
Chiang, K.-S., Bock, C. H., El Jarroudi, M., Delfosse, P., Lee, I. H., and Liu, H. I. 2016a. Effects of rater bias and assessment method on disease severity estimation with regard to hypothesis testing. Plant Pathol. 65: 523-535.
Chiang, K. S., Bock, C. H., Lee, I.-H., El Jarroudi, M., and Delfosse, P. 2016b. Plant disease severity assessment—How rater bias, assessment method and experimental design affect hypothesis testing and resource use efficiency. Phytopathology 106:1451-1464.
Chiang, K. S., Liu, H. I., and Bock, C. H. 2017a. A discussion on disease severity index values. Part I: Warning on inherent errors and suggestions to maximize accuracy. Ann. Appl. Biol. 171:139-154.
Chiang, K. S., Liu, H. I., Chen, Y. L., El Jarroudi, M., and Bock, C. H. 2020. Quantitative ordinal scale estimates of plant disease severity: Comparing treatments using a proportional odds model. Phytopathology 110:734-743.
Chiang, K. S., Liu, H. I., Tsai, J. W., Tsai, J. R., and Bock, C. H. 2017b. A discussion on disease severity index values. Part II: Using the disease severity index for null hypothesis testing. Ann. Appl. Biol. 171:490-505.
Chiang, K.-S., Liu, S.-C., Bock, C. H., and Gottwald, T. R. 2014. What interval characteristics make a good categorical disease assessment scale? Phytopathology 104:575-585.
Delignette-Muller, M. L., and Dutang, C. 2015. fitdistrplus: An R package for fitting distributions. J. Stat. Software 64:1-34.
Del Ponte, E. M., Cazón, L. I., Alves, K. S., Pethybridge, S. J., and Bock, C. H. 2022. How much do standard area diagrams improve accuracy of visual estimates of plant disease severity? A systematic review and meta-analysis. Trop. Plant Pathol. 47:43-57.
El Jarroudi, M., Kouadio, A. L., Mackels, C., Tychon, B., Delfosse, P., and Bock, C. H. 2015. A comparison between visual estimates and image analysis measurements to determine septoria leaf blotch severity in winter wheat. Plant Pathol. 64:355-364.
Esgario, J. G., Krohling, R. A., and Ventura, J. A. 2020. Deep learning for classification and severity estimation of coffee leaf biotic stress. Comput. Electron. Agric. 169:105162.
Fay, M. P., and Shaw, P. A. 2010. Exact and asymptotic weighted log rank tests for interval censored data: The interval R package. J. Stat. Software 36:1-34.
Finkelstein, D. M. 1986. A proportional hazards model for interval-censored failure time data. Biometrics 42:845-854.
Fleming, T. R., and Harrington, D. P. 1981. A class of hypothesis tests for one and two sample censored survival data. Commun. Stat. Theory Methods 10:763-794.
Forbes, G. A., and Korva, J. T. 1994. The effect of using a Horsfall–Barratt scale on precision and accuracy of visual estimation of potato late blight severity in the field. Plant Pathol. 43:675-682.
Gottwald, T. R., Hall, D. G., Kriss, A. B., Salinas, E. J., Parker, P. E., Beattie, G. A. C., and Nguyen, M. C. 2014. Orchard and nursery dynamics of the effect of interplanting citrus with guava for huanglongbing, vector, and disease management. Crop Prot. 64:93-103.
Hartung, K., and Piepho, H. P. 2007. Are ordinal rating scales better than percent ratings? A statistical and “psychological” view. Euphytica 155:15-26.
Hau, B., Kranz, J., and König, R. 1989. Fehler beim Schätzen von Befallsstärken bei Pflanzenanzenkrankheiten/Errors in the assessment of plant disease severities. Z. Pflanzenkrankh. Pflanzenschutz 96:649-674.
Horsfall, J. G., and Barratt, R. W. 1945. An improved grading system for measuring plant disease. (Abstr.). Phytopathology 35:655.
Kleinbaum, D. G., and Klein, M. 2012. Survival Analysis: A Self-Learning Text, 3rd ed. Springer-Verlag, New York.
Kranz, J. 1977. A study on maximum severity in plant disease. Pages 169-173 in: Travaux dédiés à G. Viennot-Bourgin. G. Viennot-Bourgin and J. Delage, eds. Société Française de Phythopathologie, Paris.
Kutner, M. H., Nachtsheim, C. J., Neter, J., and Li, W. 2005. Applied Linear Statistical Models, 5th ed. McGraw-Hill, New York.
Lamari, L. 2002. ASSESS: Image Analysis Software for Plant Disease Quantification. American Phytopathological Society, St. Paul, MN.
Law, C. G., and Brookmeyer, R. 1992. Effects of mid-point imputation on the analysis of doubly censored data. Stat. Med. 11:1569-1578.
Liu, H. I., Tsai, J. R., Chung, W. H., Bock, C. H., and Chiang, K. S. 2019. Effects of quantitative ordinal scale design on the accuracy of estimates of mean disease severity. Agronomy 9:565.
Madden, L. V., Hughes, G., and van den Bosch, F. 2007. The Study of Plant Disease Epidemics. American Phytopathological Society, St. Paul, MN.
Nita, M., Ellis, M. A., and Madden, L. V. 2003. Reliability and accuracy of visual estimation of Phomopsis leaf blight of strawberry. Phytopathology 93:995-1005.
Nutter, F. W., Jr., and Esker, P. D. 2006. The role of psychophysics in phytopathology: The Weber–Fechner law revisited. Eur. J. Plant Pathol. 114: 199-213.
Nutter, F. W., Jr., Gleason, M. L., Jenco, J. H., and Christians, N. C. 1993. Assessing the accuracy, intra-rater repeatability, and inter-rater reliability of disease assessment system. Phytopathology 83:806-812.
Nutter, F. W., Jr., Teng, P. S., and Shokes, F. M. 1991. Disease assessment terms and concepts. Plant Dis. 75:1187-1188.
Ojiambo, P. S., and Kang, E. L. 2013. Modeling spatial frailties in survival analysis of cucurbit downy mildew epidemics. Phytopathology 103: 216-227.
Ojiambo, P. S., and Scherm, H. 2005. Survival analysis of time to abscission of blueberry leaves affected by Septoria leaf spot. Phytopathology 95: 108-113.
Onofri, A., Mesgaran, M. B., and Ritz, C. 2022. A unified framework for the analysis of germination, emergence, and other time-to-event data in weed science. Weed Sci. 70:259-271.
Onofri, A., Piepho, H.-P., and Kozak, M. 2019. Analyzing censored data in agricultural research: A review with examples and software tips. Ann. Appl. Biol. 174:3-13.
Panageas, K. S., Ben-Porat, L., Dickler, M. N., Chapman, P. B., and Schrag, D. 2007. When you look matters: The effect of assessment schedule on progression-free survival. J. Natl. Cancer Inst. 99:428-432.
Pethybridge, S. J., Ngugi, H. K., and Hay, F. S. 2010. Use of survival analysis to assess management options for ray blight in Australian pyrethrum fields. Plant Pathol. 59:480-491.
Peto, R. 1973. Experimental survival curves for interval-censored data. J. R. Stat. Soc. Ser. C Appl. Stat. 22:86-91.
Peto, R., and Peto, J. 1972. Asymptotically efficient rank invariant test procedures. J. R. Stat. Soc. Ser. A Gen. 135:185-207.
R Core Team. 2021. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
Scherm, H., and Ojiambo, P. S. 2004. Applications of survival analysis in botanical epidemiology. Phytopathology 94:1022-1026.
Sun, J. 1996. A non-parametric test for interval-censored failure time data with application to AIDS studies. Stat. Med. 15:1387-1395.
Thomas, S., Behmann, J., Steier, A., Kraska, T., Muller, O., Rascher, U., and Mahlein, A.-K. 2018. Quantitative assessment of disease severity and rating of barley cultivars based on hyperspectral imaging in a non-invasive, automated phenotyping platform. Plant Methods 14:45.
Turnbull, B. W. 1976. The empirical distribution with arbitrarily grouped, censored and truncated data. J. R. Stat. Soc. Ser. B Methodol. 38: 290-295.
Wamonje, F. O., Donnelly, R., Tungadi, T. D., Murphy, A. M., Pate, A. E., Woodcock, C., Caulfield, J., Mutuku, J. M., Bruce, T. J. A., Gilligan, C. A., Pickett, J. A., and Carr, J. P. 2020. Different plant viruses induce changes in feeding behavior of specialist and generalist aphids on common bean that are likely to enhance virus transmission. Front. Plant Sci. 10: 1811.
Wickham, H. 2016. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York.
Yadav, N. V. S., de Vos, S. M., Bock, C. H., and Wood, B. W. 2013. Development and validation of standard area diagrams to aide assessment of pecan scab symptoms on pecan fruit. Plant Pathol. 62:325-335.