Slaving and release in co-infection control

Particle and Fibre Toxicology

Archie CA Clements¹  Juan Antonio Solon²  Kate Halton³  Darren J Gray⁴  Gail M Williams¹  Laith Yakob¹ 

[1] Infectious Disease Epidemiology Unit, School of Population Health, University of Queensland, Herston, Brisbane, Qld 4006, Australia;College of Public Health, University of the Philippines Manila, 625 Pedro Gil Street, Ermita, Manila, Philippines;Institute of Health and Biomedical Innovation, Queensland University of Technology, Kelvingrove, Qld 4059, Australia;Molecular Parasitology Laboratory, Queensland Institute of Medial Research, Herston, Brisbane, Qld 4029, Australia

关键词: Drug resistance;    Next generation matrix;    Epidemiology;    Infectious disease;    Mathematical model;    Nematode;   

Others  :  1227025
DOI  :  10.1186/1756-3305-6-157

 received in 2013-03-01, accepted in 2013-05-23,  发布年份 2013

【 摘 要 】

Background

Animal and human infection with multiple parasite species is the norm rather than the exception, and empirical studies and animal models have provided evidence for a diverse range of interactions among parasites. We demonstrate how an optimal control strategy should be tailored to the pathogen community and tempered by species-level knowledge of drug sensitivity with use of a simple epidemiological model of gastro-intestinal nematodes.

Methods

We construct a fully mechanistic model of macroparasite co-infection and use it to explore a range of control scenarios involving chemotherapy as well as improvements to sanitation.

Results

Scenarios are presented whereby control not only releases a more resistant parasite from antagonistic interactions, but risks increasing co-infection rates, exacerbating the burden of disease. In contrast, synergisms between species result in their becoming epidemiologically slaved within hosts, presenting a novel opportunity for controlling drug resistant parasites by targeting co-circulating species.

Conclusions

Understanding the effects on control of multi-parasite species interactions, and vice versa, is of increasing urgency in the advent of integrated mass intervention programmes.

【 授权许可】

   
2013 Yakob et al.; licensee BioMed Central Ltd.

【 图 表 】

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【 参考文献 】

• [1]Petney TN, Andrews RH: Multiparasite communities in animals and humans: frequency, structure and pathogenic significance. Int J Parasitol 1998, 28:377-393.
• [2]Chan MS: The global burden of intestinal nematodes infections – fifty years on. Parasitol Today 1997, 13:438-443.
• [3]Brooker S: Estimating the global distribution and disease burden of intestinal nematode infections: Adding up the numbers – A review. Int J Parasitol 2010, 40:1137-1144.
• [4]Pullan RBS: The global limits and population at risk of soil-transmitted helminth infections in 2010. Parasit Vectors 2012, 5(1):81.
• [5]Cox FEG: Concomitant infections, parasites and immune responses. Parasitology 2001, 122(Suppl):S23-S38.
• [6]Graham AL: Ecological rules governing helminth–micro parasite co infection. Proc Natl Acad Sci 2008, 105:566-570.
• [7]Pullan R, Brooker S: The health impact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases? Parasitology 2008, 135:783-794.
• [8]Brooker S, Kabatereine NB, Fleming F, Devlin N: Cost and cost–effectiveness of nationwide school-based helminth control in Uganda: intra-country variation and effects of scaling-up. Health Policy Plan 2008, 23:24-35.
• [9]Mathers CD, Ezzatti M, Lopez AD: Measuring the burden of neglected tropical diseases: the global burden of disease framework. PLoS Negl Trop Dis 2007, 1:E114.
• [10]Brooker S, Clements ACA: Spatial heterogeneity of parasite co-infection: determinants and geostatistical prediction at regional scales. Int J Parasitol 2009, 39:591-597.
• [11]Clements ACA, Deville MA, Ndayishimiye O, Fenwick A: Spatial co-distribution of neglected tropical diseases in the East African Great Lakes Region: Revisiting the justification for integrated control. Trop Med Int Health 2010, 15:198-207.
• [12]Utzinger J, De Savigny D: Control of neglected tropical diseases: integrated chemotherapy and beyond. PLoS Med 2006, 3:e112.
• [13]Mwinzi PMS, Owaga C, Mwanje M, Muok E, Ayisi J, Laserson K, Muchiri E, Secor W, Karanja D: Integrated community-directed intervention for schistosomiasis and soil transmitted helminths in western Kenya - a pilot study. Parasit Vectors 2012, 5(1):182.
• [14]Keiser J, Utzinger J: Efficacy of current drugs against soil-transmitted helminth infections: systematic review and meta-analysis. J Am Med Assoc 2008, 299:1937-1948.
• [15]Besier B: New anthelmintics for livestock: the time is right. Trends Parasitol 2007, 23:21-24.
• [16]Waller PJ: Anthelmintic resistance. Vet Parasitol 1997, 72:391-412.
• [17]Albonico M, Engels D, Savioli L: Monitoring drug efficacy and early detection of drug resistance in human soil-transmitted nematodes: a pressing public health agenda for helminth control. Int J Parasitol 2004, 34:1205-1210.
• [18]Medley GF, Guyatt HL, Bundy DAP: A quantitative framework for evaluating the effect of community treatment on the morbidity due to ascariasis. Parasitology 1993, 106:201-221.
• [19]Smith G: A mathematical model for the evolution of anthelmintic resistance in a direct life cycle nematode parasite. Int J Parasitol 1990, 20:913-921.
• [20]Anderson RM, May RM: Helminth Infections of Humans: Mathematical Models, Population Dynamics, and Control. Adv Parasitol 1985, 24:1-101.
• [21]Churcher TS, Filipe JAN, Basáñez M-G: Density dependence and the control of helminth parasites. J Anim Ecol 2006, 75:1313-1320.
• [22]Behnke JM, Wahid FN, Grencis RK, Else KJ, Ben-Smith A, Goyal PK: Immunological relationships during primary infection with Heligmosomoides polygyrus (Nematospiroides dubius): down regulation of specific cytokine secretion (IL-9 and IL-10) correlates with poor mastocytosis and chronic survival of adult worms. Parasite Immunol 1993, 15:415-421.
• [23]Behnke JM: Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions or pure randomness? Parasitology 2008, 135:751-766.
• [24]Hermanek J, Goyal PK, Wakelin D: Lymphocyte, antibody and cytokine responses during concurrent infections between helminths that selectively promote T-helper-1 or T-helper-2 activity. Parasite Immunol 1994, 16:111-117.
• [25]Christensen NO, Nansen P, Fagbemi BO, Monrad J: Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental-infection of mammalian hosts. Parasitol Res 1987, 73:387-410.
• [26]Fleming FM, Brooker S, Geiger SM, Caldas IR, Correa-Oliveira R, Hotez PJ, Bethony JM: Synergistic associations between hookworm and other helminth species in a rural community in Brazil. Trop Med Int Health 2006, 11:56-64.
• [27]Webster M, Correa-Oliveira R, Gazzinelli G, Viana IRC, Fraga LADO, Silveira AMS, Dunne DW: Factors affecting high and low human IgE responses to schistosome worm antigens in an area of Brazil endemic for Schistosoma mansoni and hookworm. AmJTrop Med Hyg 1997, 57(4):487-494.
• [28]Anderson RM, May RM: Regulation and stability of host-parasite population interactions: I. Regulatory processes. J Anim Ecol 1978, 47:219-247.
• [29]Dobson AP: The population-dynamics of competition between parasites. Parasitology 1985, 91:317-347.
• [30]Roberts MG, Dobson AP: The population-dynamics of communities of parasitic helminths. Math Biosci 1995, 126:191-214.
• [31]Gatto M, DeLeo GA: Interspecific competition among macro parasites in a density-dependent host population. J Math Biol 1998, 37:467-490.
• [32]Pugliese A: Coexistence of macro parasites without direct interactions. Theor Popul Biol 2000, 57:145-165.
• [33]Fenton A: Worms and germs: the population dynamic consequences of microparasite-macroparasite co-infection. Parasitology 2008, 135:1545-1560.
• [34]Bottomley C, Isham VS, Basáñez M-G: Population biology of multispecies helminth infection: interspecific interactions and parasite distribution. Parasitology 2005, 131:417-433.
• [35]Fenton A, Viney ME, Lello J: Detecting interspecific macro parasite interactions from ecological data: patterns and process. Ecol Lett 2010, 13:606-615.
• [36]Anderson RM, May RM: Infectious Diseases of Humans: Dynamics and Control. Oxford and New York: Oxford University Press; 1991:467-529.
• [37]Hoagland KE, Schad GA: Necator americanus and Ancylostoma duodenale: Life history parameters and epidemiological implications of two sympatric hookworms of humans. Exp Parasitol 1978, 44:36-49.
• [38]Udonsi JK, Atata G: Necator americanus: Temperature, pH, light, and larval development, longevity, and desiccation tolerance. Exp Parasitol 1987, 63(2):136-142.
• [39]Woolhouse MEJ, Dye C, Etard J-F, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JLK, Ndhlovu PD, Quinnell RJ, et al.: Heterogeneities in the transmission of infectious agents: Implications for the design of control programs. Proc Natl Acad Sci 1997, 94:338-342.
• [40]Hudson PJ, Dobson AP: Macroparasites: Observed Patterns. In Ecology of Infectious Diseases in Natural Populations. Edited by Grenfell BT, Dobson AP. Cambridge: Cambridge University Press; 1995:144-176.
• [41]Keymer AE: Density-dependent mechanisms in the regulation of intestinal helminth populations. Parasitology 1982, 84:573-587.
• [42]Chylinski C, Boag B, Stear MJ, Cattadori IM: Effects of host characteristics and parasite intensity on growth and fecundity of Trichostrongylus retortaeformis infections in rabbits. Parasitology 2009, 136(01):117-123.
• [43]Paterson S, Viney ME: Host immune responses are necessary for density dependence in nematode infections. Parasitology 2002, 125:283-292.
• [44]Grenfell BT, Wilson K, Isham VS, Boyd HEG, Dietz K: Modelling patterns of parasite aggregation in natural populations: trichostrongylid nematode-ruminant interactions as a case study. Parasitology 1995, 111(Suppl):S135-S151.
• [45]Quinnell RJ, Keymer AE, Medley GF: The regulation of gastrointestinal helminth populations. Phil Trans Roy Soc B 1990, 330:191-201.
• [46]Galvani AP: Immunity, antigenic heterogeneity, and aggregation of helminth parasites. J Parasitol 2003, 89:232-241.
• [47]Dash KM: Interaction between Oesophagostomum columbianum and Oesophagostomum venulosum in sheep. Int J Parasitol 1981, 11:201-207.
• [48]Holland C: Interactions between Moniliformis (Acanthocephala) and Nippostrongylus (Nematoda) in the small intestine of laboratory rats. Parasitology 1984, 88:303-315.
• [49]Poulin R: Interactions between species and the structure of helminth communities. Parasitology 2001, 122:S3-S11.
• [50]Howard SC, Donnelly CA, Chan MS: Methods for estimation of associations between multiple species parasite infections. Parasitology 2001, 122:233-251.
• [51]Poulin R: Detection of interspecific competition in parasite communities. J Parasitol 2005, 91(5):1232-1235.
• [52]Behnke JM, Ali NMH, Jenkins SN: Survival to patency of low-level infections with Trichuris muris in mice concurrently infected with Nematospiroides dubius. Annals Trop Med Hyg 1984, 78:509-517.
• [53]Yoshida A, Maruyama H, Yabu Y, Amano T, Kobayakawa T, Ohta N: Immune responses against protozoal and nematodal infection in mice with underlying Schistosoma mansoni infection. Parasitol Int 1999, 48:73-79.
• [54]Holmes JC: Effects of concurrent infections on Hymenolepis diminta (Cestoda) and Moniliformis dubius (Acanthocephala). II. Effects on growth. J Parasitol 1962, 48:87-96.
• [55]Holmes JC: Effects of concurrent infections on Hymenolepis diminta (Cestoda) and Moniliformis dubius (Acanthocephala). II. Effects in hamsters. J Parasitol 1962, 48:97-100.
• [56]Jones KE, Patel NG, Levy MA, Storeygard A, Balk D, Gittleman JL, Daszak P: Global trends in emerging infectious diseases. Nature 2008, 451:990-993.
• [57]Basáñez M-G, French MD, Walker M, Churcher TS: Paradigm lost: how parasite control may alter pattern and process in human helminthiases. Trends Parasitol 2012, 28:161-171.