title: Forcing versus feedback: epidemic malaria and monsoon rains in northwest India.
abstract: Malaria epidemics in regions with seasonal windows of transmission can vary greatly in size from year to year. A central question has been whether these interannual cycles are driven by climate, are instead generated by the intrinsic dynamics of the disease, or result from the resonance of these two mechanisms. This corresponds to the more general inverse problem of identifying the respective roles of external forcings vs. internal feedbacks from time series for nonlinear and noisy systems. We propose here a quantitative approach to formally compare rival hypotheses on climate vs. disease dynamics, or external forcings vs. internal feedbacks, that combines dynamical models with recently developed, computational inference methods. The interannual patterns of epidemic malaria are investigated here for desert regions of northwest India, with extensive epidemiological records for Plasmodium falciparum malaria for the past two decades. We formulate a dynamical model of malaria transmission that explicitly incorporates rainfall, and we rely on recent advances on parameter estimation for nonlinear and stochastic dynamical systems based on sequential Monte Carlo methods. Results show a significant effect of rainfall in the inter-annual variability of epidemic malaria that involves a threshold in the disease response. The model exhibits high prediction skill for yearly cases in the malaria transmission season following the monsoonal rains. Consideration of a more complex model with clinical immunity demonstrates the robustness of the findings and suggests a role of infected individuals that lack clinical symptoms as a reservoir for transmission. Our results indicate that the nonlinear dynamics of the disease itself play a role at the seasonal, but not the interannual, time scales. They illustrate the feasibility of forecasting malaria epidemics in desert and semi-arid regions of India based on climate variability. This approach should be applicable to malaria in other locations, to other infectious diseases, and to other nonlinear systems under forcing.
authors.affiliation: Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, Michigan, USA.
authors.forename: Karina
authors.initials: K
authors.lastname: Laneri
authors.forename: Anindya
authors.initials: A
authors.lastname: Bhadra
authors.forename: Edward L
authors.initials: EL
authors.lastname: Ionides
authors.forename: Menno
authors.initials: M
authors.lastname: Bouma
authors.forename: Ramesh C
authors.initials: RC
authors.lastname: Dhiman
authors.forename: Rajpal S
authors.initials: RS
authors.lastname: Yadav
authors.forename: Mercedes
authors.initials: M
authors.lastname: Pascual
mesh_terms: D000818:Animals; D003198:Computer Simulation; D009033:Culicidae; D016208:Databases, Factual; D058872:Epidemics; D025461:Feedback, Physiological; D006790:Host-Parasite Interactions; D006801:Humans; D007194:India / Q000453:epidemiology; D007303:Insect Vectors; D016778:Malaria, Falciparum / Q000453:epidemiology* / Q000635:transmission; D008954:Models, Biological; D015233:Models, Statistical; D010963:Plasmodium falciparum / Q000254:growth & development*; D011891:Rain; D012621:Seasons; D049490:Systems Biology / Q000379:methods
references.citation: Proc Natl Acad Sci U S A. 2006 Dec 5;103(49):18860-5
references.pmid: 17116860
references.citation: Stat Med. 2003 May 30;22(10):1709-24
references.pmid: 12720306
references.citation: Am J Trop Med Hyg. 1949 Jan;29(1):1-17
references.pmid: 18110328
references.citation: Science. 2006 Dec 1;314(5804):1442-5
references.pmid: 17138899
references.citation: Proc Biol Sci. 2008 Jan 22;275(1631):123-32
references.pmid: 17999952
references.citation: Nature. 2005 Aug 4;436(7051):696-700
references.pmid: 16079845
references.citation: Proc Natl Acad Sci U S A. 1994 Apr 26;91(9):3715-9
references.pmid: 8170975
references.citation: J R Soc Interface. 2008 Feb 6;5(19):247-52
references.pmid: 17698477
references.citation: J R Soc Interface. 2007 Aug 22;4(15):625-36
references.pmid: 17301013
references.citation: PLoS Med. 2009 Nov;6(11):e1000185
references.pmid: 19918362
references.citation: Science. 2001 Jul 27;293(5530):638-43
references.pmid: 11474099
references.citation: PLoS Med. 2005 Jul;2(7):e174
references.pmid: 16013892
references.citation: Am Nat. 2002 May;159(5):469-81
references.pmid: 18707430
references.citation: Am J Trop Med Hyg. 2004 Aug;71(2 Suppl):128-35
references.pmid: 15331828
references.citation: Lancet. 1994 Dec 10;344(8937):1638-9
references.pmid: 7984012
references.citation: Science. 2000 Jan 28;287(5453):667-70
references.pmid: 10650003
references.citation: Theor Popul Biol. 2001 Aug;60(1):59-71
references.pmid: 11589638
references.citation: Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):9335-9
references.pmid: 10922081
references.citation: Nat Med. 1999 Mar;5(3):340-3
references.pmid: 10086393
references.citation: Trends Parasitol. 2007 Jun;23(6):243-6
references.pmid: 17412641
references.citation: Nature. 2002 Feb 7;415(6872):710-5
references.pmid: 11832960
references.citation: Malar J. 2008 Apr 25;7:67
references.pmid: 18439283
references.citation: Am J Trop Med Hyg. 2006 Aug;75(2 Suppl):19-31
references.pmid: 16931812
references.citation: Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):13110-5
references.pmid: 16924109
references.citation: Proc Natl Acad Sci U S A. 2006 Dec 5;103(49):18438-43
references.pmid: 17121996
references.citation: Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2375-80
references.pmid: 14983017
references.citation: Nature. 2001 Dec 13;414(6865):716-23
references.pmid: 11742391
references.citation: PLoS Med. 2009 Nov;6(11):e1000168
references.pmid: 19918363
references.citation: J R Soc Interface. 2010 Feb 6;7(43):309-19
references.pmid: 19570798
references.citation: Trends Parasitol. 2001 Feb;17(2):95-9
references.pmid: 11228016
references.citation: J R Soc Interface. 2008 Aug 6;5(25):885-97
references.pmid: 18174112
references.citation: J Infect Dis. 1999 Apr;179(4):989-95
references.pmid: 10068596
references.citation: Am J Trop Med Hyg. 2005 Jul;73(1):214-21
references.pmid: 16014862
references.citation: J R Soc Interface. 2010 Feb 6;7(43):271-83
references.pmid: 19535416
references.citation: Ecology. 2009 Apr;90(4):888-900
references.pmid: 19449681
references.citation: Parasitol Today. 1999 Mar;15(3):105-11
references.pmid: 10322323
references.citation: Lancet. 1996 Nov 23;348(9039):1457-8
references.pmid: 8937310
references.citation: Bull World Health Organ. 1974;50(3-4):347-57
references.pmid: 4613512
references.citation: J Infect Dis. 2009 Jul 1;200(1):66-74
references.pmid: 19476434
references.citation: Ecology. 2009 Apr;90(4):906-12
references.pmid: 19449684
references.citation: Nature. 2008 Aug 14;454(7206):877-80
references.pmid: 18704085
references.citation: PLoS Med. 2005 Apr;2(4):e106
references.pmid: 15839751
references.citation: Trends Parasitol. 2001 Sep;17(9):438-45
references.pmid: 11530356
references.citation: Science. 2000 Sep 8;289(5485):1766-9
references.pmid: 10976073
references.citation: Parasitol Today. 1996 Jun;12(6):236-40
references.pmid: 15275204