Critical transitions in malaria transmission models are consistently generated by superinfection

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 374, Issue 1775, 2019, Pages

  Alonso, David ^a   Dobson, Andy ^b,c   Pascual, Mercedes ^c,d  

^a CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

^b PRINCETON UNIVERSITY   (United States)

^c SANTA FE INSTITUTE   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

Alternative steady states; Backward bifurcation; Critical transitions; Hysteresis in malaria model; Malaria dynamics; Malaria superinfection

Indexed keywords

DISEASE TRANSMISSION; DISEASE VECTOR; ETIOLOGY; HYSTERESIS; IMMUNE RESPONSE; INFECTIOUS DISEASE; MALARIA; MOSQUITO;

ANIMALIA;

ANIMAL; HUMAN; MALARIA; MOSQUITO; MOSQUITO VECTOR; PHYSIOLOGY; POPULATION DYNAMICS; STATISTICAL MODEL; SUPERINFECTION;

ANIMALS; CULICIDAE; HUMANS; MALARIA; MODELS, STATISTICAL; MOSQUITO VECTORS; POPULATION DYNAMICS; SUPERINFECTION;

EID: 85065417010     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2018.0275     Document Type: Article

References (50)

1. Scheffer M. 2009 Critical transition in nature and society. Princeton, NJ: Princeton University Press.
2. Chitnis N, Cushing JM, Hyman JM. 2006 Bifurcation analysis of a mathematical model for malaria transmission. SIAM J. Appl. Math. 67, 24-45. (doi:10.1137/050638941)
3. Lavine JS, King Aa, Bjørnstad ON. 2011 Natural immune boosting in pertussis dynamics and the potential for long-term vaccine failure. Proc. Natl Acad. Sci. USA 108, 7259-7264. (doi:10.1073/pnas. 1014394108)
4. Lavine JS, King AA, Andreasen V, Bjørnstad ON. 2013 Immune boosting explains regime-shifts in prevaccine-era pertussis dynamics. PLoS ONE 8, e72086. (doi:10.1371/journal.pone.0072086)
5. Jenkins R, Omollo R, Ongecha M, Sifuna P, Othieno C, Ongeri L, Kingora J, Ogutu B. 2015 Prevalence of malaria parasites in adults and its determinants in malaria endemic area of Kisumu County, Kenya. Malar. J. 14, 263. (doi:10.1186/s12936-015-0781-5)
6. Ghansah A et al. 2017 Seasonal variation in the epidemiology of asymptomatic Plasmodium falciparum infections across two catchment areas in Bongo district, Ghana. Am. J. Trop. Med. Hyg. 97, 199-212. (doi:10.4269/ajtmh.16-0959)
7. Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. 2012 Ross, MacDonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 8, e1002588. (doi:10.1371/journal.ppat.1002588)
8. Reiner RC et al. 2013 A systematic review of mathematical models of mosquito-borne pathogen transmission: 1970-2010. J. R. Soc. Interface 10, 20120921. (doi:10.1098/rsif.2012.0921)
9. Keegan LT, Dushoff J. 2013 Population-level effects of clinical immunity to malaria. BMC Infect. Dis. 13, 428. (doi:10.1186/1471-2334-13-428) ´
10. Aguas R, White LJ, Snow RW, Gomes MGM. 2008 Prospects for malaria eradication in sub-Saharan Africa. PLoS ONE 3, e1767. (doi:10.1371/journal. pone.0001767)
11. Alonso D, Bouma MJ, Pascual M. 2011 Epidemic malaria and warmer temperatures in recent decades in an East African highland. Proc. R. Soc. B 278, 1661-1669. (doi:10.1098/rspb.2010.2020)
12. Ross R. 1911 The prevention of malaria. 2nd edn. London, UK: J. Murray.
13. Ross R. 1916 An application of the theory of probabilities to the study of a priori pathometry. Proc. R. Soc. Lond. A 92, 204-230. (doi:10.1098/ rspa.1916.0007)
14. MacDonald G. 1952 Ross's a priori Pathometry-a perspective. Trop. Dis. Bull. 49, 813-829.
15. Fine PEM. 1975 A challenge for epidemiology: Ross's a priori Pathometry-a perspective. Proc. R. Soc. Med. 68, 547-551.
16. Lindblade KA, Steinhardt L, Samuels A, Kachur SP, Slutsker L. 2013 The silent threat: asymptomatic parasitemia and malaria transmission. Expert Rev. Anti Infect. Ther. 11, 623-639. (doi:10.1586/ eri.13.45)
17. Nkumama IN, O'Meara WP, Osier FHA. 2017 Changes in malaria epidemiology in Africa and new challenges for elimination. Trends Parasitol. 33, 128-140. (doi:10.1016/j.pt.2016.11.006)
18. Ghansah A et al. 2017 Seasonal variation in the epidemiology of asymptomatic Plasmodium falciparum infections across two catchment areas in Bongo District, Ghana. Am. J. Trop. Med. Hyg. 97, 199-212. (doi:10.4269/ajtmh.16-0959)
19. Dietz K, Molineax L, Thomas A. 1974 Malaria model tested in African savannah. Bull. World Health Org. 50, 347-357.
20. Aron JL, May RM. 1982 The population dynamics of malaria. In Population dynamics and infectious diseases (ed. RM Anderson), pp. 139-179. London, UK: Chapman and Hall.
21. Brauer F, Castillo-Chavez C, Mubayi A, Towers S. 2016 Some models for epidemics of vector-transmitted diseases. Infect. Dis. Model. 1, 79-87. (doi:10.1016/j.idm.2016.08.001)
22. Ross R. 1910 The prevention of malaria. London, UK: J. Murray.
23. MacDonald G. 1957 The epidemiology of malaria. London, UK: Oxford University Press.
24. Smith DL, McKenzie FE, Snow RW, Hay SI. 2007 Revisiting the basic reproductive number for malaria and its implications for malaria control. PLoS Biol. 5, e42. (doi:10.1371/journal.pbio.0050042)
25. Burden RL, Faires DJ. 1985 Numerical analysis. 3rd edn. Boston, MA: PWS Publishing Company.
26. Iooss G, Joseph DD. 1980 Elementary stability and bifurcation theory. New York, NY: Springer.
27. Anderson RM, May RM. 1991 Infectious diseases of humans. Dynamics and control. Oxford, UK: Oxford University Press.
28. 0 in models for infectious diseases in heterogeneous populations. J. Math. Biol. 28, 365-382. (doi:10.1007/BF00178324)
29. Lloyd AL. 2001 Realistic distributions of infectious periods in epidemic models: changing patterns of persistence and dynamics. Theor. Popul. Biol. 60, 59-71. (doi:10.1006/tpbi.2001.1525)
30. Medley GF, Lindop N, Edmunds W, Nokes D. 2001 Hepatitis-B virus endemicity: heterogeneity, catastrophic dynamics and control. Nat. Med. 7, 619-624. (doi:10.1038/87953)
31. Struik SS, Riley EM. 2004 Does malaria suffer from lack of memory. Immunol. Rev. 201, 268-290. (doi:10.1111/j.0105-2896.2004.00181.x)
32. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, Peterson DS, Ravetch JA, Wellems TE. 1995 The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82, 89-100. (doi:10.1016/0092-8674(95)90055-1)
33. Gupta S, Trenholme K, Anderson RM, Day KP. 1994 Antigenic diversity and the transmission dynamics of Plasmodium falciparum. Science 263, 961-963. (doi:10.1126/science.8310293)
34. Day KP et al. 2017 Evidence of strain structure in Plasmodium falciparum var gene repertoires in children from Gabon, West Africa. Proc. Natl Acad. Sci. USA 114, 201613018. (doi:10.1073/pnas.1708236114)
35. Geiger C, Agustar HK, Compaoré G, Coulibaly B, Sié A, Becher H, Lanzer M, Jänisch T. 2013 Declining malaria parasite prevalence and trends of asymptomatic parasitaemia in a seasonal transmission setting in North-Western Burkina Faso between 2000 and 2009-2012. Malar. J. 12, 27. (doi:10.1186/1475-2875-12-27)
36. Gerardin J, Ouédraogo AL, McCarthy K, Eckhoff P, Wenger E. 2015 Characterization of the infectious reservoir of malaria with an agent-based model calibrated to age-stratified parasite densities and infectiousness. Malar. J. 14, 231. (doi:10.1186/ s12936-015-0751-y)
37. Futse JE, Brayton KA, Dark MJ, Knowles DP, Palmer GH. 2008 Superinfection as a driver of genomic diversification in antigenically variant pathogens. Proc. Natl Acad. Sci. USA 105, 2123-2127. (doi:10. 1073/pnas.0710333105)
38. Smith D et al. 2013 A sticky situation: the unexpected stability of malaria elimination. Phil. Trans. R. Soc. B 368, 1623. (doi:10.1098/rstb.2012.0145)
39. Baeza A, Bouma MJ, Dhiman RC, Baskerville EB, Ceccato P, Yadav RS, Pascual M. 2013 Long-lasting transition toward sustainable elimination of desert malaria under irrigation development. Proc. Natl Acad. Sci. USA 110, 15 157 - 15 162. (doi:10.1073/ pnas.1305728110)
40. Gupta S, Maiden MCJ, Feavers IM, Nee S, May RM, Anderson RM. 1996 The maintenance of strain structure in populations of recombining infectious agents. Nat. Med. 2, 437-442. (doi:10.1038/ nm0496-437)
41. Artzy-Randrup Y, Rorick MM, Day K, Chen D, Dobson AP, Pascual M. 2012 Population structuring of multicopy, antigen-encoding genes in Plasmodium falciparum. eLife 1, e00093. (doi:10.7554/eLife.00093)
42. He Q, Pilosof S, Tiedje KE, Ruybal-Pesántez S, Artzy-Randrup Y, Baskerville EB, Day KP, Pascual M. 2018 Networks of genetic similarity reveal non-neutral processes shape strain structure in Plasmodium falciparum. Nat. Commun. 9, 1817. (doi:10.1038/ s41467-018-04219-3)
43. Karl S, White MT, Milne GJ, Gurarie D, Hay SI, Barry AE, Felger I, Mueller I, Marinho CR. 2016 Spatial effects on the multiplicity of Plasmodium falciparum infections. PLoS ONE 11, 1-20. (doi:10.1371/ journal.pone.0164054)
44. Águas R, White LJ, Snow RW, Gomes MGM. 2008 Prospects for malaria eradication in sub-Saharan Africa. PLoS ONE 3, 1 - 6. (doi:10.1371/journal.pone.0001767)
45. Echhoff P. 2013 Mathematical models of within-host and transmission dynamics to determine effects of malaria interventions in a variety of transmission settings. Am. J. Trop. Med. Hyg. 88, 817-827. (doi:10.4269/ajtmh.12-0007)
46. Chaves LF, Pascual M. 2007 Comparing models for early warning systems of neglected tropical diseases. PLoS Negl. Trop. Dis. 1, e33. (doi:10.1371/ journal.pntd.0000033)
47. Scheffer M et al. 2009 Early-warning signals for critical transitions. Nature 461, 53-59. (doi:10. 1038/nature08227)
48. Kéfi S et al. 2014 Early warning signals of ecological transitions: methods for spatial patterns. PLoS ONE 9, 10-13. (doi:10.1371/ journal.pone.0092097)
49. Brett TS, Drake JM, Rohani P. 2017 Anticipating the emergence of infectious diseases. J. R. Soc. Interface 14, 20170115. (doi:10.1098/rsif.2017.0115)
50. D'Souza K, Epureanu BI, Pascual M. 2015 Forecasting bifurcations from large perturbation recoveries in feedback ecosystems. PLoS ONE 10, 1-19. (doi:10. 1371/journal.pone.0137779)