The serial and generation intervals from SARS-CoV-2 transmission dynamics and their potential application in the epidemiology of two citrus diseases

Oscar Pérez-Hernández, Francisco Sautua, Santiago Domínguez-Monge, Carlos Cecilio Góngora-Canul, Marcelo Carmona

Abstract


Since the start of the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causing the coronavirus disease 2019 (COVID-19) pandemic, the concepts of serial and generation intervals have been used as key epidemiological measures to understand the transmission dynamics of the disease. We carefully examined and repurposed these concepts to the understanding of the transmission chain and dynamics of two major citrus diseases: tristeza virus (caused by Citrus tristeza virus, CTV) and Huanglongbing (caused by Candidatus Liberibacter asiaticus). Following the fundamental definition of the concepts, the review delineates the transmission chain in the SARS-CoV-2 and that of CTV and CLas, pointing out their major similarities and differences. Then, it discusses estimation of the serial and generation intervals and their distributions for both plant diseases. Identification of infector-infectee tree pairs in a transmission chain within orchards is proposed through use of disease incidence data from intensive mapping, spatial pattern analysis, conditional probability, and simulation approaches. Like in SARS-CoV-2 dynamics, pre-symptomatic transmission in these two plant pathosystems is of epidemiological significance. Hence, estimation of the serial and generation interval can lay the foundations to understanding of early disease transmission dynamics, thus the implementation of vector control measures or eradication of infected trees. We hope this review motivates discussions on estimation and usage of these concepts to enhance understanding of the epidemiology of both of the herein examined citrus diseases.


Keywords


COVID-19; spatial pattern; CTV; HLB; Monte Carlo simulation

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References


Agrios GN. 2005. Plant Pathology. Fifth ed. Academic Press. Burlington, Massachusetts, United States of America. https://doi.org/10.1016/C2009-0-02037-6

Asselah T, Durantel D, Pasmant E, Lau G and Schinazi RF. 2021. COVID-19: Discovery, diagnostics and drug development. Journal of Hepatology 74(1):168-184. http://dx.doi.org/10.1016/j.jhep.2020.09.031

Balaraman K and Ramakrishnan K. 1979. Transmission studies with strains of citrus tristeza virus on acid lime (Citrus aurantifolia). Journal of Plant Diseases and Protection 86: 653-661. Link: https://www.jstor.org/stable/43214591?seq=1

Bové JM. 2006. Huanglongbing: a destructive, newly emerging, century-old disease of citrus. Journal of Plant Pathology 88:7-37. http://dx.doi.org/10.4454/jpp.v88i1.828

Canale MC, Tomaseto AF, Haddad ML, Della Coletta-Filho H and Lopes JR. 2017. Latency and Persistence of 'Candidatus Liberibacter asiaticus' in Its Psyllid Vector, Diaphorina citri (Hemiptera: Liviidae). Phytopathology 107: 264-272. https://doi.org/10.1094/PHYTO-02-16-0088-R

Canale MC, Komada KMA and Lopes JRS. 2020. Latency and incubation of ‘Candidatus Liberibacter asiaticus’ in citrus after vector inoculation. Tropical plant pathology 45: 320–326. https://doi.org/10.1007/s40858-019-00311-1

Dala-Paula BM, Plotto A, Bai J, Manthey JA, Baldwin EA, Ferrarezi RS and Gloria MBA. 2019. Effect of Huanglongbing or Greening Disease on Orange Juice Quality, a Review. Frontiers in Plant Science 9:1976. https://doi.org/10.3389/fpls.2018.01976

Dawson WO, Garnsey SM, Tatineni S, Folimonova SY, Harper SJ and Gowda S. 2013. Citrus tristeza virus-host interactions. Frontiers in Microbiology 4:88. https://doi.org/10.3389/fmicb.2013.00088

Dawson WO, Bar-Joseph M, Garnsey SM and Moreno P. 2015. Citrus tristeza virus: making an ally from an enemy. Annual Review of Phytopathology 53: 137-55. https://doi.org/10.1146/annurev-phyto-080614-120012

Ferretti L, Wymant C, Kendall M, Zhao L, Nurtay A, Abeler-Dörner L, Parker M, Bonsall D and Fraser C. 2020. Quantifying SARS-CoV-2 transmission suggests epidemic control with digital contact tracing Science 368 (6491). https://doi.org/10.1126/science.abb6936

Fishman S, Marcus R, Talpaz H, Bar-Joseph M, Oren Y, Salomon R and Zohar M. 1983. Epidemiological and economic models for spread and control of citrus tristeza virus disease. Phytoparasitica 11: 1. https://doi.org/10.1007/BF02980710

Flores-Sánchez JL, Mora-Aguilera G, Loeza-Kuk E, López-Arroyo JI, Gutiérrez-Espinosa MA, Domínguez-Monge S, Bassanezi RB, Acevedo-Sánchez G and Robles-García P. 2017. Diffusion model for describing the regional spread of Huanglongbing from first-reported outbreaks and basing an area wide disease management strategy. Plant Disease 101 (7): 1119-1127. https://doi.org/10.1094/PDIS-04-16-0418-RE

Galdeano DM, de Souza Pacheco I, Alves GR, Moreira GL, Rashidi M, Turner D, Levy A and Machado MA. 2020. Friend or foe? Relationship between ‘Candidatus Liberibacter asiaticus’ and Diaphorina citri. Tropical plant pathology 45: 559–571. https://doi.org/10.1007/s40858-020-00375-4

Ganyani T, Kremer C, Chen D, Torneri A, Faes C, Wallinga J and Hens N. 2020. Estimating the generation interval for COVID-19 based on symptom onset data. MedRxiv 2020.03.05.20031815. https://doi.org/10.1101/2020.03.05.20031815

Gottwald TR, Aubert B and Zhao X-Y. 1989. Preliminary analysis of citrus greening (Huanglongbing) epidemics in the People’s Republic of China and French Reunion Island. Phytopathology 79: 687–93. http://dx.doi.org/10.1094/Phyto-79-687

Gottwald TR, da Graça JV and Bassanezi RB. 2007. Citrus Huanglongbing: The pathogen and its impact. Online. Plant Health Progress. https://doi.org/10.1094/PHP-2007-0906-01-RV

Gottwald TR, Garnsey SM and Borbón J. 1998. Increase and patterns of spread of citrus tristeza virus infections in Costa Rica and the Dominican Republic in the presence of the brown citrus aphid, Toxoptera citricida. Phytopathology 88:621-636. https://doi.org/10.1094/PHYTO.1998.88.7.621

Gottwald TR, Garnsey SM and Riley TD. 2002. Latency of Systemic Infection in Young Field-Grown Sweet Orange Trees Following Graft-Inoculation with Citrus tristeza virus. Fifteenth International Organization of Citrus Virologists Conference Proceedings (1957-2010) 15(15): 48-53. Link: https://escholarship.org/uc/item/9rb677sf

Gottwald TR, Gibson GJ, Garnsey SM and Irey M. 1999. Examination of the effect of aphid vector population composition on the spatial dynamics of citrus tristeza virus spread by stochastic modeling. Phytopathology 89(7): 603-8. https://doi.org/10.1094/PHYTO.1999.89.7.603

Gottwald T, Parnell S, Taylor E, Poole K, Hodge J, Ford A, Therrien L, Mayo S and Irey M. 2008. Within-tree spatial distribution of Candidatus Liberibacter asiaticus. Proceeding of the International Research Conference Huanglongbing, pp. 270–73. http://www.plantmanagementnetwork.org/proceedings/irchlb/2008/

Gottwald TR. 2010. Current Epidemiological Understanding of Citrus Huanglongbing. Annual Review of Phytopathology 48: 119–39. https://doi.org/10.1146/annurev-phyto-073009-114418

Gottwald T, Poole G, McCollum T, Hall D, Hartung J, Bai J, Luo W, Posny D, Duan YP, Taylor E, da Graça J, Polek M, Louws F and Schneider W. 2020. Canine olfactory detection of a vectored phytobacterial pathogen, Liberibacter asiaticus, and integration with disease control. Proceedings of the National Academy of Sciences of the United States of America 117(7): 3492?3501. https://doi.org/10.1073/pnas.1914296117

Grandjean D, Sarkis R, Lecoq-Julien C, Benard A, Roger V, Levesque E, et al. 2020. Can the detection dog alert on COVID-19 positive persons by sniffing axillary sweat samples? A proof-of-concept study. PLoS ONE 15(12): e0243122. https://doi.org/10.1371/journal.pone.0243122

Grandjean D, Marzooqi DHA, Lecoq-Julien C, et al. 2021. Use Of Canine Olfactory Detection For COVID-19 Testing Study On U.A.E. Trained Detection Dog Sensitivity. bioRxiv 2021.01.20.427105. https://doi.org/10.1101/2021.01.20.427105

Hall DG, Richardson ML, Ammar E and Halbert SE. 2013. Asian citrus psyllid, Diaphorina citri, vector of citrus huanglongbing disease. Entomolgia Experimentalis et Applicata 146: 207-223. https://doi.org/10.1111/eea.12025

Hernandez GA. 2013. Prevalencia de Toxoptera citricida y tasa de adquisición del Citrus tristeza virus en la Península de Yucatán. Tesis de maestría. Colegio de Postgraduados, México. Link: https://www.repositorionacionalcti.mx/recurso/oai:colposdigital.colpos.mx:10521/2066

Huang Z, Rundell PA, Guan X and Powell CA. 2004. Detection and Isolate Differentiation of Citrus tristeza virus in Infected Field Trees Based on Reverse Transcription-Polymerase Chain Reaction. Plant Disease 88(6): 625-629. https://doi.org/10.1094/PDIS.2004.88.6.625

Hughes G, Gottwald TR. 1998. Survey methods for assessment of citrus tristeza virus incidence. Phytopathology 88: 715-723. https://doi.org/10.1094/PHYTO.1998.88.7.715

Irey MS, Gast T and Gottwald TR. 2006. Comparison of visual assessment and polymerase chain reaction assay testing to estimate the incidence of the Huanglongbing pathogen in commercial Florida citrus. Proceedings of Florida State Horticultural Society 119:89–93

Jendrny, P., Schulz, C., Twele, F. et al. 2020. Scent dog identification of samples from COVID-19 patients – a pilot study. BMC Infectious Diseases 20: 536. https://doi.org/10.1186/s12879-020-05281-3

Johansson MA, Quandelacy TM, Kada S, et al. 2021. SARS-CoV-2 Transmission from People Without COVID-19 Symptoms. JAMA Netw Open 4(1): e2035057. https://doi.org/10.1001/jamanetworkopen.2020.35057

Keremane ML, Ramadugu C, Rodriguez E, Kubota R, Shibata S, Hall DG, Roose ML, Jenkins D and Lee RF. 2015. A rapid field detection system for citrus huanglongbing associated ‘Candidatus Liberibacter asiaticus’ from the psyllid vector, Diaphorina citri Kuwayama and its implications in disease management. Crop Protection 68: 41-48. https://doi.org/10.1016/j.cropro.2014.10.026

Kobori Y, Nakata T, Ohto Y and Takasu F. 2010. Dispersal of adult Asian citrus psyllid Diaphorina citri Kuwayama (Homoptera: Psyllidae), the vector of citrus greening disease, in artificial release experiments. Applied Entomology and Zoology. https://doi.org/10.1007/s13355-010-0004-z

Korkmaz S, Cevik B, Onder S, Koc K and Bozan O. 2008. Detection of Citrus tristeza virus (CTV) from Satsuma Owari mandarins (Citris unshiu) by direct tissue blot immunoassay (DTBIA), DAS?ELISA, and biological indexing. New Zealand Journal of Crop and Horticultural Science 36: 239-246. https://doi.org/10.1080/01140670809510240

Lee JA, Halbert SE, Dawson WO, Roberton CJ, Keesling JE and Singer BH. 2015. Asymptomatic spread of huanglongbing and implications for disease control. Proceedings of the National Academy of Sciences. 112: 7605-7610. https://doi.org/10.1073/pnas.1508253112

Lee RF, Baker PS and Rocha-Peña MA. 1994. The Citrus Tristeza Virus (CTV). Intl. Inst. Biological Control, CAB International, Silwood Park, UK. 197 p.

Lehtinen S, Ashcroft P and Bonhoeffer S. 2021. On the relationship between serial interval, infectiousness profile and generation time. Journal of the Royal Society Interface 18:20200756. https://doi.org/10.1098/rsif.2020.0756

Leung KY, Trapman P and Britton T. 2018. Who is the infector? Epidemic models with symptomatic and asymptomatic cases. Mathematical Biosciences 301: 190-198. https://doi.org/10.1016/j.mbs.2018.04.002

Li Q, Guan X, Wu P, Wang X, Zhou L, Tong Y, et al. 2020. Early Transmission Dynamics in Wuhan, China, of Novel Coronavirus-Infected Pneumonia. The New England Journal of Medicine 382(13): 1199-207. https://doi.org/10.1056/NEJMoa2001316

Li M, Liu K, Song Y, Wang M and Wu J. 2021. Serial Interval and Generation Interval for Imported and Local Infectors, Respectively, Estimated Using Reported Contact-Tracing Data of COVID-19 in China. Frontiers in Public Health 8: 577431. https://doi.org/10.3389/fpubh.2020.577431

Manjunath KL, Halbert SE, Ramadugu C, Webb S and Lee RF. 2008. Detection of 'Candidatus Liberibacter asiaticus' in Diaphorina citri and its importance in the management of citrus huanglongbing in Florida. Phytopathology 98(4): 387-396. https://doi.org/10.1094/PHYTO-98-4-0387

Mavrodiev EV, Turskly ML, Mavrodiev NE, Ebach MC and Williams DM. 2020. On classification and taxonomy of Coronaviruses (Riboviria, Nidovirales, Coronaviridae) with the special focus on severe acute respiratory syndrome related coronavirus 2 (SARS-Cov-2). https://doi.org/10.1101/2020.10.17.343749

Mettler SK, Kim J and Maathuis MH. 2020. Diagnostic serial interval as a novel indicator for contact tracing effectiveness exemplified with the SARS-CoV-2/COVID-19 outbreak in South Korea. International Journal of Infectious Diseases 99: 346-351. https://doi.org/10.1016/j.ijid.2020.07.068

Mora-Aguilera G, Ochoa-Martínez DL, Gutiérrez-Espinosa MA, Villegas MA, Álvarez-Ramos R, Jasso J, Góngora-Canul CC, Ruiz-García N, Rivas-Valencia P, Loeza-Kuk E, Palacios TC, Pérez Molphe-Bach E, Febres V, Moore G, Moreno P, Mendoza A and Quiroz J. 2005. Citrus tristeza closterovirus: consideraciones biológicas y epidemiológicas. pp. 1-25. In: Memorias del IX Simposio Internacional de citricultura. 19-23 abril. Cd. Victoria, Tamaulipas. México.

Mora-Aguilera G. 2008. Bases de estudios epidemiológicos para el manejo de patosistemas agrícolas. Taller internacional de vigilancia epidemiológica fitosanitaria para el pronóstico de plaga. México. Link: http://langif.uaslp.mx/documentos/presentaciones_internacionl/01/drmora.pdf

Moreno P, Ambros S, Albiach-Marti MR, Guerri J and Pena L. 2008. Citrus tristeza virus: a pathogen that changed the course of the citrus industry. Molecular Plant Pathology 9: 251–268. https://doi.org/10.1111/j.1364-3703.2007.00455.x

Ng SH, Kaur P, Kremer C, Tan WS, Tan AL, Hens N, Toh MP, Teow KL and Kannapiran P. 2021. Estimating transmission parameters for COVID-19 clusters by using symptom onset data, Singapore, January–April 2020. 27: 582-585. https://doi.org/10.3201/eid2702.203018

Nishiura H, Linton NM and Akhmetzhanov AR. 2020. Serial interval of novel coronavirus (COVID-19) infections. International Journal of Infectious Diseases 93: 284-286. https://doi.org/10.1016/j.ijid.2020.02.060

Prather KA, Wang CC and Schooley RT. 2020. Reducing transmission of SARS-CoV-2. Science 368(6498): 1422-1424. https://doi.org/10.1126/science.abc6197

Qian G, Yang N, Ma AHY, Wang L, Li G, Chen X, et al. 2020. A COVID-19 Transmission within a family cluster by presymptomatic infectors in China. Clinical Infectious Diseases 71:861–2. https://doi.org/10.1093/cid/ciaa316

Rimbaud L, Dallot S, Delaunay A, Borron S, Soubeyrand S, Thébaud G and Jacquot E. 2015. Assessing the Mismatch Between Incubation and Latent Periods for Vector-Borne Diseases: The Case of Sharka. Phytopathology 105(11): 1408-16. https://doi.org/10.1094/PHYTO-01-15-0014-R

Rivas-Valencia P, Loeza-Kuk E, Domínguez-Monge S and Lomas-Barrié CT. 2017. Infección crónica del virus de la tristeza de los cítricos en árboles de Citrus sinensis/C. aurantium en un régimen térmico restrictivo en Yucatán. Revista Chapingo. Serie horticultura 23(3): 188-202. https://doi.org/10.5154/r.rchsh.2016.11.028

Rivas-Valencia P, Domínguez-Monge S, Santillán-Mendoza R, Loeza-Kuk E, Pérez-Hernández O, Rodríguez-Quibrera C and Lomas-Barrié C. 2020. Severe Citrus tristeza virus Isolates from Eastern Mexico Are Related to the T36 Genotype Group. American Journal of Plant Sciences 11: 1521-1532. https://doi.org/10.4236/ajps.2020.1110110.

Rocha-Peña MA, Lee RF, Lastra R, Niblett CL, Ochoa-Corona FM, Garnsey SM and Yokomi RK 1994. Citrus Tristeza Virus and Its Aphid Vector Toxoptera citricida: Threats to Citrus Production in the Caribbean and Central and North America. Plant Disease 79(5): 437-444. https://doi.org/10.1094/PD-79-0437

Rosa C, Polek M, Falk BW and Rowhani A. 2007. Improved Efficiency for Quantitative and Qualitative Indexing for Citrus tristeza virus and Citrus psorosis virus. Plant Disease 91(9): 1089-1095. https://doi.org/10.1094/PDIS-91-9-1089

Rothman KJ, Lash T and Greenland S. 2012. Modern Epidemiology, third ed. Lippincott Williams & Wilkins. ISBN: 9781451190052. 758 p.

Ruiz-Ruiz S, Moreno P, Guerri J and Ambrós S. 2007. A real-time RT-PCR assay for detection and absolute quantitation of Citrus tristeza virus in different plant tissues. Journal of Virological Methods 145: 96-105. https://doi.org/10.1016/j.jviromet.2007.05.011

Saponari M, Manjunath K and Yokomi RK. 2008. Quantitative detection of Citrus tristeza virus in citrus and aphids by real-time reverse transcription-PCR (TaqMan). Journal of Virological Methods 147(1): 43-53. https://doi.org/10.1016/j.jviromet.2007.07.026

Spreen TH, Baldwin J and Futch SH. 2014. An Economic Assessment of the Impact of Huanglongbing on Citrus Tree Plantings in Florida, HortScience 49(8): 1052-1055. Retrieved Feb 15, 2021, from https://journals.ashs.org/hortsci/view/journals/hortsci/49/8/article-p1052.xml

te Beest DE, Wallinga J, Donker T and van Boven M. 2013. Estimating the generation interval of influenza A (H1N1) in a range of social settings. Epidemiology 24(2): 244-50. https://doi.org/10.1097/EDE.0b013e31827f50e8

Torres-Pacheco I, Lopez-Arroyo JI, Aguirre-Gómez JA, Guevara-González RG, Yanez-López R, Hernández-Zul MI and Quijano-Carranza JA. 2013. Potential distribution of Diaphorina citri (Hemiptera: Psyllidae) vector of huanglongbing in Mexico. Florida Entomologist 96: 36-47 https://doi.org/10.1653/024.096.0105

Wei W, Li Z, Chiew C, Yong S, Toh M and Lee V. 2020. Presymptomatic transmission of SARS-CoV-2–Singapore, January 23 March 16, 2020. MMWR Morb Mortal Wkly Rep. 69:411–5. https://doi.org/10.15585/mmwr.mm6914el

Wu Y, Chen C and Chan Y. 2020. The outbreak of COVID-19: An overview Journal of Chinese Medical Association 83: 217-220. https://doi.org/10.1097/JCMA.0000000000000270

Yokomi R, Lastra R, Stoetzel MB, Damsteegt VD, Lee RF, Garnsey SM, Gottwald TR, Rocha-Peña MA and Niblett CL. 1994. Establishment of the brown citrus aphid (Homoptera: Aphididae) in Central America and the Caribbean basin and Transmission of citrus tristeza virus. Journal of Economic Entomology 87: 1078-1085. https://doi.org/10.1093/jee/87.4.1078




DOI: http://dx.doi.org/10.18781/R.MEX.FIT.2021-23

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