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Differential drivers of intraspecific and interspecific competition during malaria–helminth co-infection

Published online by Cambridge University Press:  11 May 2021

L. F. Wait Open the ORCID record for L. F. Wait [Opens in a new window] ,
T. Kamiya ,
K. J. Fairlie-Clarke ,
C. J. E. Metcalf ,
A. L. Graham  and
N. Mideo
L. F. Wait*
Affiliation:
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, USA
T. Kamiya
Affiliation:
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada
K. J. Fairlie-Clarke
Affiliation:
Roslin Technologies Ltd, Edinburgh, UK
C. J. E. Metcalf
Affiliation:
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, USA
A. L. Graham
Affiliation:
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, USA
N. Mideo
Affiliation:
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, Ontario, Canada
*
Author for correspondence: L. F. Wait, E-mail: lwait@princeton.edu
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Abstract

Various host and parasite factors interact to determine the outcome of infection. We investigated the effects of two factors on the within-host dynamics of malaria in mice: initial infectious dose and co-infection with a helminth that limits the availability of red blood cells (RBCs). Using a statistical, time-series approach to model the within-host ‘epidemiology’ of malaria, we found that increasing initial dose reduced the time to peak cell-to-cell parasite propagation, but also reduced its magnitude, while helminth co-infection delayed peak cell-to-cell propagation, except at the highest malaria doses. Using a mechanistic model of within-host infection dynamics, we identified dose-dependence in parameters describing host responses to malaria infection and uncovered a plausible explanation of the observed differences in single vs co-infections. Specifically, in co-infections, our model predicted a higher background death rate of RBCs. However, at the highest dose, when intraspecific competition between malaria parasites would be highest, these effects of co-infection were not observed. Such interactions between initial dose and co-infection, although difficult to predict a priori, are key to understanding variation in the severity of disease experienced by hosts and could inform studies of malaria transmission dynamics in nature, where co-infection and low doses are the norm.

Keywords

Co-infectiondose dependencehookworminfectious dosemalariawithin-host
Type
Research Article
Information
Parasitology , Volume 148 , Issue 9 , August 2021 , pp. 1030 - 1039
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Abel, L and Desseint, AJ (1997) The impact of host genetics on susceptibility to human infectious diseases. Current Opinion in Immunology 9, 509–516.CrossRefGoogle ScholarPubMed
Aparecida, D, Neto, MB, De Paula, NT, Tolardo, L and Yokosawa, J (2014) Human rhinovirus and disease severity in children. Pediatrics 133, e312–e321.Google Scholar
Bichet, C, Larcombe, S, Faivre, B and Sorci, G (2014) Impact of host nutritional status on infection dynamics and parasite virulence in a bird-malaria system. Journal of Animal Ecology 83, 256–265.Google Scholar
Bouchery, T, Filbey, K, Shepherd, A, Chandler, J, Patel, D, Schmidt, A, Camberis, M, Peignier, A, Smith, AAT, Johnston, K, Painter, G, Pearson, M, Giacomin, P, Loukas, A, Bottazzi, ME, Hotez, P and LeGros, G (2018) A novel blood-feeding detoxification pathway in Nippostrongylus brasiliensis L3 reveals a potential checkpoint for arresting hookworm development. PLoS Pathogens 14, 1–20.CrossRefGoogle ScholarPubMed
Brunner, JL, Richards, K and Collins, JP (2005) Dose and host characteristics influence virulence of ranavirus infections. Oecologia 144, 399–406.CrossRefGoogle ScholarPubMed
Budischak, SA, Wiria, AE, Hamid, F, Wammes, LJ, Kaisar, MMM, van Lieshout, L, Sartono, E, Supali, T, Yazdanbakhsh, M and Graham, AL (2018) Competing for blood: the ecology of parasite resource competition in human malaria-helminth co-infections. Ecology Letters 21, 536–545. doi: 10.1111/ele.12919CrossRefGoogle ScholarPubMed
Carpenter, B, Gelman, A, Hoffman, MD, Lee, D, Goodrich, B, Betancourt, M, Brubaker, MA, Li, P and Riddell, A (2017) Stan : a probabilistic programming language. Journal of Statistical Software 76, 1–32.CrossRefGoogle Scholar
Cox, FEG (2001) Concomitant infections, parasites and immune responses. Parasitology 122, S23–S38.CrossRefGoogle ScholarPubMed
Eswarappa, SM, Estrela, S and Brown, SP (2012) Within-host dynamics of multi-species infections: facilitation, competition and virulence. PLoS ONE 7, e38730. doi: 10.1371/journal.pone.0038730CrossRefGoogle ScholarPubMed
Ezenwa, VO, Etienne, RS, Luikart, G, Beja-Pereira, A and Jolles, AE (2010) Hidden consequences of living in a wormy world: nematode-induced immune suppression facilitates Tuberculosis invasion in African buffalo. The American Naturalist 176, 613–624.CrossRefGoogle Scholar
Fairlie-Clarke, KJ, Hansen, C, Allen, JE and Graham, AL (2015) Increased exposure to Plasmodium chabaudi antigens sustains cross-reactivity and avidity of antibodies binding Nippostrongylus brasiliensis: dissecting cross-phylum cross-reactivity in a rodent model. Parasitology 142, 1703–1714.CrossRefGoogle Scholar
Fenton, A and Perkins, SE (2010) Applying predator-prey theory to modelling immune-mediated, within-host interspecific parasite interactions. Parasitology 137, 1027–1038.CrossRefGoogle ScholarPubMed
Fenton, A, Knowles, SCL, Petchey, OL and Pedersen, AB (2014) The reliability of observational approaches for detecting interspecific parasite interactions : comparison with experimental results. International Journal for Parasitology 44, 437–445.CrossRefGoogle ScholarPubMed
Foster, H, Small, J and Fox, J (2014) Hematology.Google Scholar
Gazzinelli, RT, Kalantari, P and Fitzgerald, KA (2014) Innate sensing of malaria parasites. Nature Reviews Immunology 14, 744–757.CrossRefGoogle ScholarPubMed
Ginzburg, LR and Jensen, CXJ (2004) Rules of thumb for judging ecological theories. Trends in Ecology and Evolution 19, 121–126.CrossRefGoogle ScholarPubMed
Griffiths, EC, Fairlie-Clarke, K, Allen, JE, Metcalf, CJE and Graham, AL (2015) Bottom-up regulation of malaria population dynamics in mice co-infected with lung-migratory nematodes. Ecology Letters 18, 1387–1396.CrossRefGoogle ScholarPubMed
Haydon, DT, Matthews, L, Timms, R and Colegrave, N (2003) Top-down or bottom-up regulation of intra-host blood-stage malaria: do malaria parasites most resemble the dynamics of prey or predator? Proceedings of the Royal Society B: Biological Sciences 270, 289–298.CrossRefGoogle ScholarPubMed
Kamiya, T, Greischar, MA, Schneider, DS and Mideo, N (2020) Uncovering drivers of dose-dependence and individual variation in malaria infection outcomes. PLoS Computational Biology 16, e1008211.CrossRefGoogle ScholarPubMed
Knowles, SCL (2011) The effect of helminth co-infection on malaria in mice: a meta-analysis. International Journal for Parasitology 41, 1041–1051.CrossRefGoogle ScholarPubMed
Kochin, BF, Yates, AJ, De Roode, JC and Antia, R (2010) On the control of acute rodent malaria infections by innate immunity. PLoS ONE 5, e10444.CrossRefGoogle ScholarPubMed
Laishram, DD, Sutton, PL, Nanda, N, Sharma, VL, Sobti, RC and Carlton, JM (2012) The complexities of malaria disease manifestations with a focus on asymptomatic malaria. Malaria Journal 11, 1–15.CrossRefGoogle ScholarPubMed
Lazzaro, BP and Little, TJ (2009) Immunity in a variable world. Philosophical Transactions of the Royal Society B: Biological Sciences 364, 15–26.CrossRefGoogle Scholar
Marois, I, Cloutier, A, Garneau, E and Richter, MV (2012) Initial infectious dose dictates the innate, adaptive, and memory responses to influenza in the respiratory tract. Journal of Leukocyte Biology 92, 107–121.CrossRefGoogle ScholarPubMed
McAlister, RO (1977) Time-dependent loss of invasive ability of Plasmodium berghei merozoites in vitro. The Journal of Parasitology 63, 455–463.CrossRefGoogle ScholarPubMed
McKenney, DG, Kurath, G and Wargo, AR (2016) Characterization of infectious dose and lethal dose of two strains of infectious hematopoietic necrosis virus (IHNV). Virus Research 214, 80–89.CrossRefGoogle Scholar
Metcalf, CJE, Graham, AL, Huijben, S, Barclay, VC, Long, GH, Grenfell, BT, Read, AF and Bjørnstad, ON (2011) Partitioning regulatory mechanisms of within-host malaria dynamics using the effective propagation number. Science (New York, N.Y.) 333, 984–988.CrossRefGoogle ScholarPubMed
Metcalf, CJE, Long, GH, Mideo, N, Forester, JD, Bjørnstad, ON and Graham, AL (2012) Revealing mechanisms underlying variation in malaria virulence: effective propagation and host control of uninfected red blood cell supply. Journal of the Royal Society Interface 9, 2804–2813.CrossRefGoogle ScholarPubMed
Mideo, N, Barclay, VC, Chan, BHK, Savill, NJ, Read, AF and Day, T (2008a) Understanding and predicting strain-specific patterns of pathogenesis in the rodent malaria Plasmodium chabaudi. The American Naturalist 172, E214–E238.CrossRefGoogle Scholar
Mideo, N, Day, T and Read, AF (2008b) Modelling malaria pathogenesis. Cellular Microbiology 10, 1947–1955.CrossRefGoogle Scholar
Mideo, N, Savill, N, Chadwick, W, Schneider, P, Read, A, Day, T and Reece, S (2011) Causes of variation in malaria infection dynamics: insights from theory and data. The American Naturalist 178, 174–188.CrossRefGoogle ScholarPubMed
Miller, LH, Baruch, DI, Marsh, K and Doumbo, OK (2002) The pathogenic basis of malaria. Nature 415, 673–679.CrossRefGoogle ScholarPubMed
Miller, MR, Raberg, L, Read, AF and Savill, NJ (2010) Quantitative analysis of immune response and erythropoiesis during rodent malarial infection. PLoS Computational Biology 6, e1000946.CrossRefGoogle ScholarPubMed
Nacher, M, Singhasivanon, P and Vannaphan, S (2001) Socio-economic and environmental protective/risk factors for severe malaria in Thailand. Acta Tropica 78, 139–146.CrossRefGoogle ScholarPubMed
Park, AW and Ezenwa, VO (2020) Characterising interactions between co-infecting parasites using age-intensity profiles. International Journal for Parasitology 50, 23–26.CrossRefGoogle ScholarPubMed
Pedersen, AB and Fenton, A (2007) Emphasizing the ecology in parasite community ecology. Trends in Ecology and Evolution 22, 133–139.CrossRefGoogle ScholarPubMed
Peron, G, de Thomaz, LL, Camargo da Rosa, L, Thome, R and Verinaud, LMC (2018) Modulation of dendritic cell by pathogen antigens: where do we stand? Immunology Letters 196, 91–102.CrossRefGoogle ScholarPubMed
Ravindran, B, Sahool, P and Dash, A (1998) Lymphatic filariasis and malaria: concomitant parasitism in Orissa, India. Transactions of the Royal Society of Tropical Medicine and Hygiene 92, 21–23.CrossRefGoogle ScholarPubMed
Savill, NJ, Chadwick, W and Reece, SE (2009) Quantitative analysis of mechanisms that govern red blood cell age structure and dynamics during anaemia. PLoS Computational Biology 5, e1000416.CrossRefGoogle ScholarPubMed
Schmid-Hempel, P and Frank, SA (2007) Pathogenesis, virulence, and infective dose. PLoS Pathogens 3, 1372–1373.CrossRefGoogle ScholarPubMed
Schmidt, C, Schneble, N and Wetzker, R (2014) The fifth dimension of innate immunity. Journal of Cell Communication and Signaling 8, 363–367.CrossRefGoogle ScholarPubMed
Stephens, R, Culleton, RL and Lamb, TJ (2015) The contribution of Plasmodium chabaudi to our understanding of malaria. Trends in Parasitology 28, 74–83.Google Scholar
Stevenson, MM and Riley, EM (2004) Innate immunity to malaria. Nature Reviews Immunology 4, 169–180.CrossRefGoogle ScholarPubMed
Timms, R, Colegrave, N, Chan, BHK and Read, AF (2001) The effect of parasite dose on disease severity in the rodent malaria Plasmodium chabaudi. Parasitology 123, 1–11.CrossRefGoogle ScholarPubMed
Tshikuka, J, Scott, M, Gray-Donald, K and Kalumba, O (1996) Multiple infection with Plasmodium and helminths in communities of low and relatively high socio-economic status. Annals of Tropical Medicine and Parasitology 90, 277–293.CrossRefGoogle ScholarPubMed
Van Putten, LM and Croon, F (1958) The life span of red cells in the rat and the mouse as determined by labeling with DFP32 in vivo. Blood 13, 789–794.CrossRefGoogle ScholarPubMed
Wale, N, Jones, MJ, Sim, DG, Read, AF and King, AA (2019) The contribution of host cell-directed vs. parasite- directed immunity to the disease and dynamics of malaria infections. Proceedings of the National Academy of Sciences 116, 13774–13779.CrossRefGoogle ScholarPubMed
Zwart, MP, Daròs, JA and Elena, SF (2011) One is enough: in vivo effective population size is dose-dependent for a plant RNA virus. PLoS Pathogens 7, e1002122. doi: 10.1371/journal.ppat.1002122CrossRefGoogle ScholarPubMed
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