Skip to main content
Springer Nature - PMC COVID-19 Collection logoLink to Springer Nature - PMC COVID-19 Collection
. 2012 Mar 1;66(3):535–546. doi: 10.1007/s00285-012-0520-2

Role of environmental persistence in pathogen transmission: a mathematical modeling approach

Romulus Breban 1,
PMCID: PMC7079992  PMID: 22382994

Abstract

Although diseases such as influenza, tuberculosis and SARS are transmitted through an environmentally mediated mechanism, most modeling work on these topics is based on the concepts of infectious contact and direct transmission. In this paper we use a paradigm model to show that environmental transmission appears like direct transmission in the case where the pathogen persists little time in the environment. Furthermore, we formulate conditions for the validity of this modeling approximation and we illustrate them numerically for the cases of cholera and influenza. According to our results based on recently published parameter estimates, the direct transmission approximation fails for both cholera and influenza. While environmental transmission is typically chosen over direct transmission in modeling cholera, this is not the case for influenza.

Keywords: Environmental transmission, Environmental persistence, Direct transmission, Slow–fast dynamics

References

  1. Anderson RM, Donnelly CA, Ferguson NM, Woolhouse ME, Watt CJ, Udy HJ, MaWhinney S, Dunstan SP, Southwood TR, Wilesmith JW, Ryan JB, Hoinville LJ, Hillerton JE, Austin AR, Wells GA. Transmission dynamics and epidemiology of BSE in British cattle. Nature. 1996;382(6594):779–788. doi: 10.1038/382779a0. [DOI] [PubMed] [Google Scholar]
  2. Ballesteros S, Vergu E, Cazelles B. Influenza A gradual and epochal evolution: insights from simple models. PLoS One. 2009;4(10):e7426. doi: 10.1371/journal.pone.0007426. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berglund N, Gentz B. Noise-induced phenomena in slow–fast dynamical systems: a sample-paths approach. Berlin: Springer; 2006. [Google Scholar]
  4. Blanchong JA, Samuel MD, Goldberg DR, Shadduck DJ, Lehr MA. Persistence of pasteurella multocida in wetlands following avian cholera outbreaks. J Wildl Dis. 2006;42(1):33–39. doi: 10.7589/0090-3558-42.1.33. [DOI] [PubMed] [Google Scholar]
  5. Breban R, Drake J, Rohani P. A general multi-strain model with environmental transmission: invasion conditions for the disease-free and endemic states. J Theor Biol. 2010;264(3):729–736. doi: 10.1016/j.jtbi.2010.03.005. [DOI] [PubMed] [Google Scholar]
  6. Breban R, Drake JM, Stallknecht DE, Rohani P. The role of environmental transmission in recurrent avian influenza epidemics. PLoS Comput Biol. 2009;5(4):e1000346. doi: 10.1371/journal.pcbi.1000346. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Caley P, Philp DJ, McCracken K. Quantifying social distancing arising from pandemic influenza. J R Soc Interface. 2008;5(23):631–639. doi: 10.1098/rsif.2007.1197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Chowell G, Nishiura H, Bettencourt LMA. Comparative estimation of the reproduction number for pandemic influenza from daily case notification data. J R Soc Interface. 2007;4(12):155–166. doi: 10.1098/rsif.2006.0161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Codeço C. Endemic and epidemic dynamics of cholera: the role of the aquatic reservoir. BMC Infect Dis. 2001;1(1):1. doi: 10.1186/1471-2334-1-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Codeço C, Lele S, Pascual M, Bouma M, Ko A. A stochastic model for ecological systems with strong nonlinear response to environmental drivers: application to two water-borne diseases. J R Soc Interface. 2008;5(19):247–252. doi: 10.1098/rsif.2007.1135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Dennis B. Allee effects: population growth, critical density, and the chance of extinction. Nat Resour Model. 1989;3(4):481–538. [Google Scholar]
  12. D’Souza DH, Sair A, Williams K, Papafragkou E, Jean J, Moore C, Jaykus L. Persistence of caliciviruses on environmental surfaces and their transfer to food. Int J Food Microbiol. 2006;108(1):84–91. doi: 10.1016/j.ijfoodmicro.2005.10.024. [DOI] [PubMed] [Google Scholar]
  13. Fenichel N. Geometric singular perturbation theory for ordinary differential equations. J Differ Equ. 1979;31(1):53–98. doi: 10.1016/0022-0396(79)90152-9. [DOI] [Google Scholar]
  14. Field H, Young P, Yob JM, Mills J, Hall L, Mackenzie J. The natural history of Hendra and Nipah viruses. Microbes Infect. 2001;3(4):307–314. doi: 10.1016/S1286-4579(01)01384-3. [DOI] [PubMed] [Google Scholar]
  15. Goldstein E, Dushoff J, Ma J, Plotkin JB, Earn DJD, Lipsitch M. Reconstructing influenza incidence by deconvolution of daily mortality time series. Proc Natl Acad Sci USA. 2009;106(51):21825–21829. doi: 10.1073/pnas.0902958106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Gralton J, Tovey E, McLaws ML, Rawlinson WD. The role of particle size in aerosolised pathogen transmission: a review. J Infect. 2011;62(1):1–13. doi: 10.1016/j.jinf.2010.11.010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Handel A, Longini IM, Antia R. What is the best control strategy for multiple infectious disease outbreaks. Proc R Soc B. 2007;274(1611):833–837. doi: 10.1098/rspb.2006.0015. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Henning J, Meers J, Davies PR, Morris RS. Survival of rabbit haemorrhagic disease virus (RHDV) in the environment. Epidemiol Infect. 2005;133(4):719–730. doi: 10.1017/S0950268805003766. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Jensen M, Faruque SM, Mekalanos JJ, Levin B. Modeling the role of bacteriophage in the control of cholera outbreaks. Proc Natl Acad Sci USA. 2006;103(12):4652. doi: 10.1073/pnas.0600166103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. King AA, Ionides EL, Pascual M, Bouma MJ. Inapparent infections and cholera dynamics. Nature. 2008;454(7206):877–880. doi: 10.1038/nature07084. [DOI] [PubMed] [Google Scholar]
  21. Li S, Eisenberg J, Spicknall I, Koopman J. Dynamics and control of infections transmitted from person to person through the environment. Am J Epidemiol. 2009;170(2):257–265. doi: 10.1093/aje/kwp116. [DOI] [PubMed] [Google Scholar]
  22. Miller MW, Hobbs NT, Tavener SJ. Dynamics of prion disease transmission in mule deer. Ecol Appl. 2006;16(6):2208–2214. doi: 10.1890/1051-0761(2006)016[2208:DOPDTI]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
  23. Pascual M, Bouma M, Dobson A. Cholera and climate: revisiting the quantitative evidence. Microbes Infect. 2002;4(2):237–245. doi: 10.1016/S1286-4579(01)01533-7. [DOI] [PubMed] [Google Scholar]
  24. Pepper IL, Rusin P, Quintanar DR, Haney C, Josephson KL, Gerba CP. Tracking the concentration of heterotrophic plate count bacteria from the source to the consumer’s tap. Int J Food Microbiol. 2004;92(3):289–295. doi: 10.1016/j.ijfoodmicro.2003.08.021. [DOI] [PubMed] [Google Scholar]
  25. Reynolds KA, Watt PM, Boone SA, Gerba CP. Occurrence of bacteria and biochemical markers on public surfaces. Int J Environ Heal R. 2005;15(3):225–234. doi: 10.1080/09603120500115298. [DOI] [PubMed] [Google Scholar]
  26. Roche B, Lebarbenchon C, Gauthier-Clerc M, Chang CM, Thomas F, Renaud F, van der Werf S, Guégan JF. Water-borne transmission drives avian influenza dynamics in wild birds: the case of the 2005–2006 epidemics in the Camargue area. Infect Genet Evol. 2009;9(5):800–805. doi: 10.1016/j.meegid.2009.04.009. [DOI] [PubMed] [Google Scholar]
  27. Rohani P, Breban R, Stallknecht DE, Drake JM. Environmental transmission of low pathogenicity avian influenza viruses and its implications for pathogen invasion. Proc Natl Acad Sci USA. 2009;106(25):10365–10369. doi: 10.1073/pnas.0809026106. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Roper MH, Vandelaer JH, Gasse FL. Maternal and neonatal tetanus. Lancet. 2007;370(9603):1947–1959. doi: 10.1016/S0140-6736(07)61261-6. [DOI] [PubMed] [Google Scholar]
  29. Rusin P, Orosz-Coughlin P, Gerba C. Reduction of faecal coliform, coliform and heterotrophic plate count bacteria in the household kitchen and bathroom by disinfection with hypochlorite cleaners. J Appl Microbiol. 1998;85(5):819–828. doi: 10.1046/j.1365-2672.1998.00598.x. [DOI] [PubMed] [Google Scholar]
  30. Sakamoto K. Invariant manifolds in singular perturbation problems for ordinary differential equations. P Roy Soc Edinb A. 1990;116(1–2):45–78. doi: 10.1017/S0308210500031371. [DOI] [Google Scholar]
  31. Spicknall IH, Koopman JS, Nicas M, Pujol JM, Li S, Eisenberg JNS. Informing optimal environmental influenza interventions: how the host, agent, and environment alter dominant routes of transmission. PLoS Comput Biol. 2010;6(10):e1000969. doi: 10.1371/journal.pcbi.1000969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Vardavas R, Breban R, Blower S. Can influenza epidemics be prevented by voluntary vaccination? PLoS Comput Biol. 2007;3(5):e85. doi: 10.1371/journal.pcbi.0030085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Webb CT, Brooks CP, Gage KL, Antolin MF. Classic flea-borne transmission does not drive plague epizootics in prairie dogs. Proc Natl Acad Sci USA. 2006;103(16):6236–6241. doi: 10.1073/pnas.0510090103. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Xiao Y, Bowers RG, Clancy D, French NP. Dynamics of infection with multiple transmission mechanisms in unmanaged/managed animal populations. Theor Popul Biol. 2007;71(4):408–423. doi: 10.1016/j.tpb.2007.02.003. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Mathematical Biology are provided here courtesy of Nature Publishing Group

RESOURCES