Abstract
Mechanistic epidemiological modelling has a role in predicting the spatial and temporal spread of emerging disease outbreaks and purposeful application of control treatment in animal populations. Especially in the case of infectious diseases newly emerging in an ecological habitat, lack of knowledge may hamper direct parameterisation of model algorithms. Along with experimental studies observational data is usually based on case notifications. These data are widely acknowledged as having “biological precision” due to e.g. convenient sampling procedures, host or human activity patterns or diagnostic limitations under field conditions. Nevertheless, the data comprises the complex spatio-temporal distribution patterns of the infection. In the literature, this data value is non-systematically used to inform model development although the need for and value of the data is well recognised. Here we address the newly emerging epidemic of African swine fever spreading in Eurasian wild boar using an existing spatio-temporally explicit individual-based model of wild boar. The disease etiology required the implementation of a sub-model regarding transmission by carcasses left after infected individuals have died. However, the experimental evidence about the mechanism involved in carcass-mediated spread of the infection still has to be established. We propose a mechanistic quantitative procedure to optimise calibration of several uncertain parameters based on the spatio-temporal model output from the simulation environment and the spatio-temporal case data of infectious disease notifications. The best agreement with the spatio-temporal spreading pattern was achieved by parameterisation that suggests ubiquitous accessibility to carcasses but with marginal chance of being contacted by conspecifics e.g., avoidance behaviour. The parameter estimation procedure is fully general and applicable to problems where spatio-temporal explicit data recording and spatial-explicit dynamic modelling was performed.
Similar content being viewed by others
References
Alban L, Andersen MM, Asferg T, Boklund A, Fernández N, Goldbach SG, Greiner M, Højgaard A, Kramer-Schadt S, Stockmarr A, Thulke HH, Uttenthal, Ydesen B (2005) Risk assessment for introduction of wild boar (Sus scrofa) to Denmark. Society for veterinary Epidemiology and Preventive Medicine. In: Proceedings of a meeting held at Nairn, Inverness, Scotland 2005:79–90
Blome S, Gabriel C, Dietze K, Breithaupt A, Beer M (2012) High virulence of African swine fever virus Caucasus isolate in European wild boars of all ages. Emerg Infect Dis 18:708
Christley RM, Mort M, Wynne B, Wastling JM, Heathwaite AL, Pickup R, Austin Z, Latham SM (2013) “Wrong, but useful”: negotiating uncertainty in infectious disease modelling. PLoS ONE 8:e76277
Coly S, Charras-Garrido M, Abrial D, Yao-Lafourcade A-F (2015) Spatiotemporal disease mapping applied to infectious diseases. Procedia Environ Sci 26:32–37
Costard S, Mur L, Lubroth J, Sanchez-Vizcaino JM, Pfeiffer DU (2013) Epidemiology of African swine fever virus. Virus Res 173:191–197
Cowled BD, Garner MG, Negus K, Ward MP (2012) Controlling disease outbreaks in wildlife using limited culling: modelling classical swine fever incursions in wild pigs in Australia. Vet Res 43:3
Cox-Witton K, Reiss A, Woods R, Grillo V, Baker RT, Blyde DJ, Boardman W, Cutter S, Lacasse C, McCracken H, Pyne M, Smith I, Vitali S, Vogelnest L, Wedd D, Phillips M, Bunn C, Post L (2014) Emerging infectious diseases in free-ranging wildlife—Australian zoo based wildlife hospitals contribute to national surveillance. PLoS ONE 9:e95127
Craft ME, Volz E, Packer C, Meyers LA (2009) Distinguishing epidemic waves from disease spillover in a wildlife population. Proc R Soc B 276:1777–1785
Dhollander S, Depner K, Belsham GJ, Salman M, Willgert K, Thulke HH, Lange M, Khomenko S, Alexandrov T, Özyörük F, Chondrokouki E, Bøtner A (2016) Evaluating the potential spread and maintenance of foot-and-mouth disease virus in wildlife; general principles and application to a specific scenario in Thrace. Transbound Emerg Dis 63:165–174
Diggle P (2006) Spatio-temporal point processes, partial likelihood, foot and mouth disease. Stat Methods Med Res 15:325–336
EFSA AHAW (2015) African swine fever: how to harmonise data collection in the Baltic countries and Poland. http://www.efsa.europa.eu/en/events/event/151123. Accessed 15 Apr 2016
EFSA AHAW Panel (2012) Scientific opinion on foot and mouth disease in Thrace. EFSA J 10:2635
EFSA AHAW Panel (2015a) Scientific opinion on African swine fever. EFSA J 13:4163
EFSA AHAW Panel (2015b) Scientific opinion on peste des petits ruminants. EFSA J 13:3985
Eisinger D, Thulke HH (2008) Spatial pattern formation facilitates eradication of infectious diseases. J Appl Ecol 45:415–423
FAO/ASFORCE (2015) Deliverable D10.5 Wild boar mapping distribution over Europe and in countries at risk based on demographic data
Fernández N, Kramer-Schadt S, Thulke HH (2006) Viability and risk assessment in species restoration: planning reintroductions for the wild boar, a potential disease reservoir. Ecol Soc 11(1):6
Gabriel C, Blome S, Malogolovkin A, Parilov S, Kolbasov D, Teifke JP, Beer M (2011) Characterization of African swine fever virus Caucasus isolate in European wild boars. Emerg Infect Dis 17:2342–2345
Garner MG, Cowled B, East IJ, Moloney BJ, Kung NY (2011) Evaluating the effectiveness of early vaccination in the control and eradication of equine influenza—a modelling approach. Prev Vet Med 99:15–27
Gavier-Widén D, Ståhl K, Neimanis AS, Hård av Segerstad C, Gortázar C, Rossi S, Kuiken T (2015) Editorial: African swine fever in wild boar in Europe: a notable challenge. Vet Rec 2015(176):199–200
Grimm V, Railsback SF (2012) Pattern-oriented modelling: a ‘multi-scope’ for predictive systems ecology. Philos Trans R Soc B 367:298–310
Grimm V, Revilla E, Berger U, Jeltsch F, Mooij WM, Railsback SF, Thulke HH, Weiner J, Wiegand T, DeAngelis DL (2005) Pattern-oriented modeling of agent-based complex systems: lessons from ecology. Science 310:987–991
Grimm V, Berger U, Bastiansen F, Eliassen S, Ginot V, Giske J, Goss-Custard J, Grand T, Heinz S, Huse G, Huth A, Jepsen JU, Jørgensen C, Mooij WM, Müller B, Pe’er G, Piou C, Railsback SF, Robbins AM, Robbins MM, Rossmanith E, Rüger N, Strand E, Souissi S, Stillman RA, Vabø R, Visser U, DeAngelis DL (2006) A standard protocol for describing individual-based and agent-based models. Ecol Model 192:115–126
Guinat C, Reis AL, Netherton CL, Goatley L, Pfeiffer DU, Dixon L (2014) Dynamics of African swine fever virus shedding and excretion in domestic pigs infected by intramuscular inoculation and contact transmission. Vet Res 45:93
Hurd HS, Kaneene JB (1993) The application of simulation models and systems analysis in epidemiology: a review. Prev Vet Med 15:81–99
Jaccard P (1912) The distribution of the flora in the alpine zone. New Phytol 11:37–50
Jeltsch F, Müller MS, Grimm V, Brandl R (1997) Pattern formation triggered by rare events: lessons from the spread of rabies. Proc R Soc B 264:495–503
Karl S, Halder N, Kelso JK, Ritchie SA, Milne GJ (2014) A spatial simulation model for dengue virus infection in urban areas. BMC Infect Dis 14(1):1
Keeling M (2006) State-of-science review: predictive and real-time epidemiological modelling. Office of Science and Innovation, London
Keeling MJ, Woolhouse MEJ, Shaw DJ, Matthews L, Chase-Topping M, Haydon DT, Cornell SJ, Kappey J, Wilesmith J, Grenfell BT (2001) Dynamics of the 2001 UK foot and mouth epidemic: stochastic dispersal in a heterogeneous landscape. Science 294:813–817
Khomenko S, Beltrán-Alcrudo D, Rozstalnyy A, Gogin A, Kolbasov D, Pinto J, Lubroth J, Martin V (2013) African swine fever in the Russian Federation: risk factors for Europe and beyond. EMPRES Watch 28:1–14
Kramer-Schadt S, Fernández N, Thulke HH (2007a) Potential ecological and epidemiological factors affecting the persistence of classical swine fever in wild boar Sus scrofa populations. Mamm Rev 37:1–20
Kramer-Schadt S, Revilla E, Wiegand T, Grimm V (2007b) Patterns for parameters in simulation models. Ecol Model 204:553–556
Kramer-Schadt S, Fernández N, Eisinger D, Grimm V, Thulke HH (2009) Individual variations in infectiousness explain long-term disease persistence in wildlife populations. Oikos 118:199–208
Lange M, Kramer-Schadt S, Thulke HH (2012) Efficiency of spatio-temporal vaccination regimes in wildlife populations under different viral constraints. Vet Res 43:37
Lange M, Siemen H, Blome S, Thulke HH (2014) Analysis of spatio-temporal patterns of African swine fever cases in Russian wild boar does not reveal an endemic situation. Prev Vet Med 117(2):317–325
Levin S (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967
Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359
Loong T (2003) Understanding sensitivity and specificity with the right side of the brain. BMJ 327:716–719
Meyer S, Elias J, Höhle M (2010) A space-time conditional intensity model for infectious disease occurrence. Technical Report Number 095. Department of Statistics, University of Munich, Munich
Moltke Jordt A, Lange M, Kramer-Schadt S, Harm Nielsen L, Saxmose Nielsen S, Thulke H-H, Vejre H, Alban L (2016) Spatio-temporal modeling of the invasive potential of wild boar—a conflict-prone species—using multi-source citizen science data. Preventive Veterinary Medicine 124:34–44
Mörner T, Obendorf DL, Artois M, Woodford MH (2002) Surveillance and monitoring of wildlife diseases. Rev Sci Tech 21:67–76
Moustakas A, Evans MR (2016) Regional and temporal characteristics of bovine tuberculosis of cattle in Great Britain. Stoch Env Res Risk Assess 30:989–1003
Oganesyan AS, Petrova ON, Korennoy FI, Bardina NS, Gogin AE, Dudnikov SA (2013) African swine fever in the Russian Federation: spatio-temporal analysis and epidemiological overview. Virus Res 173:204–211
OIE (2014) Disease distribution map: African swine fever in domestic and wild pigs, January 2013 to August 2014. Accessed 10 Aug 2014 World Animal Health Information Database of the World Organisation for Animal Health, http://web.oie.int/
Penrith ML, Vosloo W (2009) Review of African swine fever: transmission, spread and control. J S Afr Vet Assoc 80:58–62
Pietschmann J, Guinat C, Beer M, Pronin V, Tauscher K, Petrov A, Keil G, Blome S (2016) Course and transmission characteristics of oral low-dose infection of domestic pigs and European wild boar with a Caucasian African swine fever virus isolate. Arch Virol 160(7):1657–1667
Premashthira S, Salman MD, Hill AE, Reich RM, Wagner BA (2011) Epidemiological simulation modeling and spatial analysis for foot-and-mouth disease control strategies: a comprehensive review. Anim Health Res Rev 12:225–234
Ray RR, Seibold H, Heurich M (2014) Invertebrates outcompete vertebrate facultative scavengers in simulated lynx kills in the Bavarian Forest National Park, Germany. Ani Biodivers Conserv 37:77–88
Riley S (2007) Large-scale spatial-transmission models of infectious disease. Science 316:1298–1301
Riley S, Eames K, Isham V, Mollison D, Trapman P (2015) Five challenges for spatial epidemic models. Epidemics 10:68–71
Sánchez-Vizcaíno JM, Mur L, Martínez-López B (2013) African swine fever (ASF) five years around Europe. Vet Microbiol 165:45–50
Selva N, Jedrzejewska B, Jedrzejewski W, Wajrak A (2005) Factors affecting carcass use by a guild of scavengers in European temperate woodland. Can J Zool 83:1590–1601
Smith DL, Lucey B, Waller LA, Childs JE, Real LA (2002) Predicting the spatial dynamics of rabies epidemics on heterogeneous landscapes. PNAS 99:3668–3672
Thrusfield M (2007) Veterinary Epidemiology. Wiley, New York
Thulke H-H, Grimm V, Müller M, Staubach C, Tischendorf L, Jeltsch F (1999) From pattern to practice: a scaling-down strategy for spatially explicit modelling illustrated by the spread and control of rabies. Ecol Model 117:179–202
Thulke H-H, Tischendorf L, Staubach C, Selhorst T, Jeltsch F, Müller T, Schlüter H, Wissel C (2000) The spatio-temporal dynamics of a post-vaccination resurgence of rabies in foxes and emergency vaccination planning. Prev Vet Med 47:1–21
Thulke HH, Selhorst T, Müller T (2005) Pseudorabies virus infections in wild boar: data visualisation as an aid to understanding disease dynamics. Prev Vet Med 68:35–48
U.S. Department of State—Humanitarian Information Unit (2013) Detailed world polygons (LSIB)—Eurasia/Africa
Vanem E (2011) Long-term time-dependent stochastic modelling of extreme waves. Stoch Environ Res Risk Assess 25:185–209
Wang JF, Guo Y-S, Christakos G, Yang W-Z, Liao Y-L, Zhong-Jie LI, Xiao-Zhou LI, Lai SJ, Chen HY (2011) Hand, foot and mouth disease: spatiotemporal transmission 665 and climate. Int J Health Geogr 10:1–10
Wiegand K, Ward D, Thulke H-H, Jeltsch F (2000) From snapshot information to long-term population dynamics of Acacias by a simulation model. Plant Ecol 150:97–114
Wiegand T, Jeltsch F, Hanski I, Grimm V (2003) Using pattern-oriented modeling for revealing hidden information: a key for reconciling ecological theory and application. Oikos 100:209–222
Wikipedia (2016) https://en.wikipedia.org/wiki/Sensitivity_and_specificity. Accessed 4 Aug 2016
Woolhouse M (2011) How to make predictions about future infectious disease risks. Philos Trans R Soc B 366:2045–2054
Acknowledgements
The authors gratefully acknowledge C. Staubach (FLI, Germany), A. Viltrop (EMU, Estonia), A. Gogin (EFSA, Italy) and S. Khomenko (FAO, Italy) for their immense support with data validation, conversion and management.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lange, M., Thulke, HH. Elucidating transmission parameters of African swine fever through wild boar carcasses by combining spatio-temporal notification data and agent-based modelling. Stoch Environ Res Risk Assess 31, 379–391 (2017). https://doi.org/10.1007/s00477-016-1358-8
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00477-016-1358-8