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Functional group/guild modelling of inter-specific pathogen interactions: A potential tool for predicting the consequences of co-infection

  • J. LELLO (a1) and T. HUSSELL (a2)


Although co-infection is the norm in most human and animal populations, clinicians currently have no practical tool to assist them in choosing the best treatment strategy for such patients. Given the vast range of potential pathogens which may co-infect the host, obtaining such a practical tool may seem an intractable problem. In ecology the joint concepts of functional groups and guilds have been used to conceptually simplify complex ecosystems, in order to understand how their component parts interact and may be manipulated. Here we propose a mechanism by which to apply these concepts to pathogen co-infection systems. Further, we describe how these groups could be incorporated into a mathematical modelling framework which, after validation, could be used as a clinical tool to predict the outcome of any particular combination of pathogens co-infecting a host.


Corresponding author

Corresponding author: Dr Joanne Lello, School of Biosciences, Cardiff University, Biomedical Sciences Building, Museum Avenue, Cardiff, CF10 3US; Tel: 02920 875885; Fax: 02920 874562; E-Mail:


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Abbassi, H., Dambrine, G., Cherel, Y., Coudert, F. and Naciri, M. (2000). Interaction of Marek's disease virus and Cryptosporidium baileyi in experimentally infected chickens. Avian Diseases 44, 776789.
Abolhassani, M. and Darabi, H. (2006). Immunosuppressive activity of Leishmania major culture supernatant. Iranian Journal of Public Health 35, 2227.
Abu-Raddad, L. J., Patnaik, P. and Kublin, J. G. (2006). Dual infection with HIV and malaria fuels the spread of both diseases in sub-Saharan Africa. Science 314, 16031606.
Allard, J. B., Poynter, M. E., Marr, K. A., Cohn, L., Rincon, M. and Whittaker, L. A. (2006). Aspergillus fumigatus generates an enhanced th2-biased immune response in mice with defective cystic fibrosis transmembrane conductance regulator. Journal of Immunology 177, 51865194.
Azevedo, M. S. P., Yuan, L., Pouly, S., Gonzales, A. M., Jeong, K. I., Nguyen, T. V. and Saif, L. J. (2006). Cytokine responses in gnotobiotic pigs after infection with virulent or attenuated human rotavirus. Journal of Virology 80, 372382.
Baumgart, M., Tompkins, F., Leng, J. and Hesse, M. (2006). Naturally occurring CD4(+)Foxp3(+) regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation. Journal of Immunology 176, 53745387.
Bayraktar, M. R., Mehmet, N. and Durmaz, R. (2005). Serum cytokine changes in Turkish children infected with Giardia lamblia with and without allergy: Effect of metronidazole treatment. Acta Tropica 95, 116122.
Becker, Y. (2006). Respiratory syncytial virus (RSV) evades the human adaptive immune system by skewing the Th1/Th2 cytokine balance toward increased levels of Th2 cytokines and IgE, markers of allergy – a review. Virus Genes 33, 235252.
Biber, P. D., Harwell, M. A. and Cropper, W. P. (2004). Modeling the dynamics of three functional groups of macroalgae in tropical seagrass habitats. Ecological Modelling 175, 2554.
Bilenko, N., Levy, A., Dagan, R., Deckelbaum, R. J., El-on, Y. and Fraser, D. (2004). Does co-infection with Giardia lamblia modulate the clinical characteristics of enteric infections in young children? European Journal of Epidemiology 19, 877883.
Blondel, J. (2003). Guilds or functional groups: does it matter? Oikos 100, 223231.
Brown, M., Mawa, P. A., Joseph, S., Bukusuba, J., Watera, C., Whitworth, J. A. G., Dunne, D. W. and Elliott, A. M. (2005). Treatment of Schistosoma mansoni infection increases helminth-specific type 2 cytokine responses and HIV-1 loads in coinfected Ugandan adults. Journal of Infectious Diseases 191, 16481657.
Cardoso, L. S., Oliveira, S. C., Pacifico, L. G. G., Goes, A. M., Oliveira, R. R., Fonseca, C. T., De Carvalho, E. M. and Araujo, M. I. (2006). Schistosoma mansoni antigen-driven interleukin-10 production in infected asthmatic individuals. Memorias do Instituto Oswaldo Cruz 101, 339343.
Carlyon, J. A. and Fikrig, E. (2003). Invasion and survival strategies of Anaplasma phagocytophilum. Cellular Microbiology 5, 743754.
Catovsky, S. (1998). Functional groups: clarifying our use of the term. Bulletin of the Ecological Society of America 79, 126127.
Christensen, N. O., Nansen, P., Fagbemi, B. O. and Monrad, J. (1987). Heterologous antagonistic and synergistic interactions between helminths and between helminths and protozoans in concurrent experimental-infection of mammalian hosts. Zeitschrift fűr Parasitenkunde-Parasitology Research 73, 387410.
Cooper, A. M., Dalton, D. K., Stewart, T. A., Griffin, J. P., Russell, D. G. and Orme, I. M. (1993). Disseminated tuberculosis in interferon-gamma gene-disrupted mice. Journal of Experimental Medicine 178, 22432247.
Coutinho, H. M., Leenstra, T., Acosta, L. P., Su, L., Jarilla, B., Jiz, M. A., Langdon, G. C., Olveda, R. M., Mcgarvey, S. T., Kurtis, J. D. and Friedman, J. F. (2006). Pro-inflammatory cytokines and C-reactive protein are associated with undernutrition in the context of Schistosoma japonicum infection. American Journal of Tropical Medicine and Hygiene 75, 720726.
D'orazio, S. E. F., Troese, M. J. and Starnbach, M. N. (2006). Cytosolic localization of Listeria monocytogenes triggers an early IFN-gamma response by CD8(+) T cells that correlates with innate resistance to infection. Journal of Immunology 177, 71467154.
Davic, R. D. (2003). Linking keystone species and functional groups: A new operational defintion of the keystone species concept. Conservation Ecology 7, r11 (online).
Davis, A. J., Liu, W. C., Perner, J. and Voigt, W. (2004). Reliability characteristics of natural functional group interaction webs. Evolutionary Ecology Research 6, 11451166.
Dawson, H. D., Beshah, E., Nishi, S., Solano-Aguilar, G., Morimoto, M., Zhao, A. P., Madden, K. B., Ledbetter, T. K., Dubey, J. P., Shea-Donohue, T., Lunney, J. K. and Urban, J. F. (2005). Localized multigene expression patterns support an evolving Th1/Th2-like paradigm in response to infections with Toxoplasma gondii and Ascaris suum. Infection and Immunity 73, 11161128.
De Bernardis, F., Lucciarini, R., Boccanera, M., Amantini, C., Arancia, S., Morrone, S., Mosca, M., Cassone, A. and Santoni, G. (2006). Phenotypic and functional characterization of vaginal dendritic cells in a rat model of Candida albicans vaginitis. Infection and Immunity 74, 42824294.
Deehan, M. R., Goodridge, H. S., Blair, D., Lochnit, G., Dennis, R. D., Geyer, R., Harnett, M. M. and Harnett, W. (2002). Immunomodulatory properties of Ascaris suum glycosphingolipids – phosphorylcholine and non-phosphorylcholine-dependent effects. Parasite Immunology 24, 463469.
Deka, S., Vanover, J., Dessus-Babus, S., Whittimore, J., Howett, M. K., Wyrick, P. B. and Schoborg, R. V. (2006). Chlamydia trachomatis enters a viable but non-cultivable (persistent) state within herpes simplex virus type 2 (HSV-2) co-infected host cells. Cellular Microbiology 8, 149162.
Dekossodo, S. and Grau, G. E. (1993). Profiles of cytokine production in relation with susceptibility to cerebral malaria. Journal of Immunology 151, 48114820.
Deschoolmeester, M. L., Manku, H. and Else, K. J. (2006). The innate immune responses of colonic epithelial cells to Trichuris muris are similar in mouse strains that develop a type 1 or type 2 adaptive immune response. Infection and Immunity 74, 62806286.
Deshpande, P. and Shastry, P. (2004). Modulation of cytokine profiles by malaria pigment – hemozoin: role of IL-10 in suppression of proliferative repsonses of mitogen stimulated human PBMC. Cytokine 28, 205213.
Diehl, S. and Rincon, M. (2002). The two faces of IL-6 on Th1/Th2 differentiation. Molecular Immunology 39, 531536.
Dumay, O., Tari, P. S., Tomasini, J. A. and Mouillot, D. (2004). Functional groups of lagoon fish species in Languedoc Roussillon, southern France. Journal of Fish Biology 64, 970983.
Dunne, D. W., Vennervald, B. J., Booth, M., Joseph, S., Fitzsimmons, C. M., Cahen, P., Sturrock, R. F., Ouma, J. H., Mwatha, J. K., Kimani, G., Kariuki, H. C., Kazibwe, F., Tukahebwa, E. and Kabatereine, N. B. (2006). Applied and basic research on the epidemiology, morbidity, and immunology of schistosomiasis in fishing communities on Lake Albert, Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 216223.
Egusa, H., Nikawa, H., Makihira, S., Yatani, H. and Hamada, T. (2006). In vitro mechanisms of interleukin-8-mediated responses of human gingival epithelial cells to Candida albicans infection. International Journal of Medical Microbiology 296, 301311.
Farouk, S. E., Dolo, A., Bereczky, S., Kouriba, B., Maiga, B., Farnert, A., Perlmann, H., Hayano, M., Montgomery, S. M., Doumbo, O. K. and Troye-Blomberg, M. (2005). Different antibody- and cytokine-mediated responses to Plasmodium falciparum parasite in two sympatric ethnic tribes living in Mali. Microbes and Infection 7, 110117.
Feng, C. G., Kaviratne, M., Rothfuchs, A. G., Cheever, A., Hieny, S., Young, H. A., Wynn, T. A. and Sher, A. (2006). NK cell-derived IFN-gamma differentially regulates innate resistance and neutrophil response in T cell-deficient hosts infected with Mycobacterium tuberculosis. Journal of Immunology 177, 70867093.
Ferrari, T. C. A., Moreira, P. R. R., Sampaio, M. J., Da Cunha, A. S., De Oliveira, J. T., Gazzinelli, G. and Correa-Oliveira, R. (2006). Intrathecal cytokines in spinal cord schistosomiasis. Journal of Neuroimmunology 177, 136141.
Foster, T. E. and Brooks, J. R. (2005). Functional groups based on leaf physiology: are they spatially and temporally robust? Oecologia 144, 337352.
Foulds, K. E., Rotte, M. J. and Seder, R. A. (2006). IL-10 is required for optimal CD8 T cell memory following Listeria monocytogenes infection. Journal of Immunology 177, 25652574.
Fowler, M. I., Yin, K., Humphries, H. E., Heckels, J. E. and Christodoulides, M. (2006). Comparison of the inflammatory responses of human meningeal cells following challenge with Neisseria lactamica and with Neisseria meningitidis. Infection and Immunity 74, 64676478.
Fulton, E. A., Parslow, J. S., Smith, A. D. M. and Johnson, C. R. (2004). Biogeochemical marine ecosystem models II: the effect of physiological detail on model performance. Ecological Modelling 173, 371406.
Furuta, T., Kikuchi, T., Iwakura, Y. and Watanabe, N. (2006). Protective roles of mast cells and mast cell-derived TNF in murine malaria. Journal of Immunology 177, 32943302.
Furze, R. C., Hussell, T. and Selkirk, M. E. (2006). Amelioration of influenza-induced pathology in mice by coinfection with Trichinella spiralis. Infection and Immunity 74, 19241932.
Gbakima, A. A. (1993). The effect of dietary-protein on Trichinella spiralis infection and inflammatory reactions in the tongue in CD1 mice. Nutrition Research 13, 787800.
Graham, A. L., Lamb, T. J., Read, A. F. and Allen, J. E. (2005). Malaria-filaria coinfection in mice makes malarial disease more severe unless filarial infection achieves patency. Journal of Infectious Diseases 191, 410421.
Gurish, M. F., Bryce, P. J., Tao, H., Kisselgof, A. B., Thornton, E. M., Miller, H. R., Friend, D. S. and Oettgen, H. C. (2004). IgE enhances parasite clearance and regulates mast cell responses in mice infected with Trichinella spiralis. Journal of Immunology 172, 11391145.
Harms, G. and Feldmeier, H. (2002). Review: HIV infection and tropical parasitic diseases – deleterious interactions in both directions? Tropical Medicine & International Health 7, 479488.
Helmby, H. and Grencis, R. K. (2002). IL-18 regulates intestinal mastocytosis and Th2 cytokine production independently of IFN-gamma during Trichinella spiralis infection. Journal of Immunology 169, 25532560.
Hood, R. R., Laws, E. A., Armstrong, R. A., Bates, N. R., Brown, C. W., Carlson, C. A., Chai, F., Doney, S. C., Falkowski, P. G., Feely, R. A., Friedrichs, M. A. M., Landry, M. R., Moore, J. K., Nelson, D. M., Richardson, T. L., Salihoglu, B., Schartau, M., Toole, D. A. and Wiggert, J. D. (2006). Pelagic functional group modeling: Progress, challenges and prospects. Deep-Sea Research Part II-Topical Studies in Oceanography 53, 459512.
Hsu, C. C. (2006). Generalizing self-organizing map for categorical data. Ieee Transactions on Neural Networks 17, 294304.
Hughes, C. A. and Shafran, S. D. (2006). Treatment of hepatitis C in HIV-coinfected patients. Annals of Pharmacotherapy 40, 479489.
Jiang, B., Snipes-Magaldi, L., Dennehy, P., Keyserling, H., Holman, R. C., Bresee, J., Gentsch, J. and Glass, R. I. (2003). Cytokines as mediators for or effectors against rotavirus disease in children. Clinical and Diagnostic Laboratory Immunology 10, 9951001.
John, C. C., Opika-Opoka, R., Byarugaba, J., Idro, R. and Boivin, M. J. (2006). Low levels of RANTES are associated with mortality in children with cerebral malaria. Journal of Infectious Diseases 194, 837845.
Karosi, T., Jokay, I., Konya, J., Szabo, L. Z., Pytel, J., Jori, J., Szalmas, A. and Sziklai, I. (2006). Detection of osteoprotegerin and TNF-alpha mRNA in ankylotic staples footplates in connection with measles virus positivity. Laryngoscope 116, 14271433.
Khan, W. I., Vallance, B. A., Blennerhasset, P. A., Deng, Y., Verdu, E. F., Matthaei, K. I. and Collins, S. M. (2001). Critical role for signal transducer and activator of transcription factor 6 in mediating intestinal muscle hypercontractility and worm expulsion in Trichinella spiralis-infected mice. Infection and Immunity 69, 838844.
King, J. R., Andersen, A. N. and Cutter, A. D. (1998). Ants as bioindicators of habitat disturbance: validation of the functional group model for Australia's humid tropics. Biodiversity and Conservation 7, 16271638.
Kontorinis, N., Agarwal, K. and Dieterich, D. T. (2005). Treatment of hepatitis C virus in HIV patients: a review. Aids 19, S166S173.
Kosonen, J., Rantala, A., Little, C. H., Lintu, P., Harjamaki, P. R., Georgiou, G. M., Cone, R. E. and Savolainen, J. (2006). Increased levels of Candida albicans mannan-specific T-cell-derived antigen binding molecules in patients with invasive candidiasis. Clinical and Vaccine Immunology 13, 467474.
Kringel, H., Iburg, T., Dawson, H., Aasted, B. and Roepstorff, A. (2006). A time course study of immunological responses in Trichuris suis infected pigs demonstrates induction of a local type 2 response associated with worm burden. International Journal for Parasitology 36, 915924.
Lello, J., Boag, B., Fenton, A., Stevenson, I. R. and Hudson, P. J. (2004). Competition and mutualism among the gut helminths of a mammalian host. Nature 428, 840844.
Li, E. Q., Zhou, P. and Singer, S. M. (2006). Neuronal nitric oxide synthase is necessary for elimination of Giardia lamblia infections in mice. Journal of Immunology 176, 516521.
Liew, F. Y., Xu, D. M., Brint, E. K. and O'neill, L. A. J. (2005). Negative regulation of Toll-like receptor-mediated immune responses. Nature Reviews Immunology 5, 446458.
Liu, Q., Liu, Z. G., Alem, F., Whitmire, J., Urban, J. and Gause, W. (2005). IL-18 induces IL-4 independent IL-13 mediated host resistance to Trichuris muris. FASEB Journal 19, A938A938.
Loeuillet, C., Martinon, F., Perez, C., Munoz, M., Thome, M. and Meylan, P. R. (2006). Mycobacterium tuberculosis subverts innate immunity to evade specific effectors. Journal of Immunology 177, 62456255.
McConchie, B. W., Norris, H. H., Bundoc, V. G., Trivedi, S., Boesen, A., Urban, J. F. and Keane-Myers, A. M. (2006). Ascaris suum-derived products suppress mucosal allergic inflammation in an interleukin-10-independent manner via interference with dendritic cell function. Infection and Immunity 74, 66326641.
Mikhailova, A. A., Belevskaya, R. G., Kalyuzhnaya, M., Fonina, L. A., Liashenko, V. A. and Petrov, R. V. (2006). Myelopeptide-2 recovers interleukin-2 synthesis and interleukin-2 receptor expression in human T lymphocytes depressed by tumor products or measles virus. Journal of Immunotherapy 29, 306312.
Milcu, A., Partsch, S., Langel, R. and Scheu, S. (2006). The response of decomposers (earthworms, springtails and microorganisms) to variations in species and functional group diversity of plants. Oikos 112, 513524.
Morales, P., Reyes, P., Vargas, M., Rios, M., Imarai, M., Cardenas, H., Croxatto, H., Orihuela, P., Vargas, R., Fuhrer, J., Heckels, J. E., Christodoulides, M. and Velasquez, L. (2006). Infection of human Fallopian tube epithelial cells with Neisseria gonorrhoeae protects cells from tumor necrosis factor alpha-induced apoptosis. Infection and Immunity 74, 36433650.
Mukherjee, P., Sen, P. C. and Ghose, A. C. (2006). Lymph node cells from BALB/c mice with chronic visceral leishmaniasis exhibiting cellular anergy and apoptosis: Involvement of Ser/Thr phosphatase. Apoptosis 11, 20132029.
Mullen, A. B., Lawrence, C. E., Mcfarlane, E., Wei, X. Q. and Carter, K. C. (2006). Endogenous interleukin-18 is involved in immunity to Leishmania donovani but its absence does not adversely influence the therapeutic activity of sodium stibogluconate. Immunology 119, 348354.
Onah, D. N. and Wakelin, D. (1999). Trypanosome-induced suppression of responses to Trichinella spiralis in vaccinated mice. International Journal for Parasitology 29, 10171026.
Ozoren, N., Masumoto, J., Franchi, L., Kanneganti, T. D., Body-Malapel, M., Erturk, I., Jagirdar, R., Zhu, L., Inohara, N., Bertin, J., Coyle, A., Grant, E. P. and Nunez, G. (2006). Distinct roles of TLR2 and the adaptor ASC in IL-1 beta/IL-18 secretion in response to Listeria monocytogenes. Journal of Immunology 176, 43374342.
Page, K. R., Scott, A. L. and Manabe, Y. C. (2006). The expanding realm of heterologous immunity: friend or foe? Cellular Microbiology 8, 185196.
Parekh, S. B., Bubb, W. A., Hunt, N. H. and Rae, C. (2006). Brain metabolic markers reflect susceptibility status in cytokine gene knockout mice with murine cerebral malaria. International Journal for Parasitology 36, 14091418.
Park, Y. S., Chon, T. S., Kwak, I. S. and Lek, S. (2004). Hierarchical community classification and assessment of aquatic ecosystems using artificial neural networks. Science of the Total Environment 327, 105122.
Parthasarathy, G. and Mansfield, L. S. (2005). Trichuris suis excretory secretory products (ESP) elicit interleukin-6 (IL-6) and IL-10 secretion from intestinal epithelial cells (IPEC-1). Veterinary Parasitology 131, 317324.
Paterson, J. C. M., Garside, P., Kennedy, M. W. and Lawrence, C. E. (2002). Modulation of a heterologous immune response by the products of Ascaris suum. Infection and Immunity 70, 60586067.
Pedersen, A. B. and Fenton, A. (2007). Emphasizing the ecology in parasite community ecology. Trends in Ecology & Evolution 22, 133139.
Pepe, M., Altamura, M., Spinelli, R., Calvello, R., Saccia, M., Cavallo, P., Covelli, V., Jirillo, E. and Brandonisio, O. (2006). Toll-like receptor-positive cells and recognition of pathogens: How human myeloid dendritic cells respond to in vitro infection with Leishmania infantum. Current Pharmaceutical Design 12, 42554262.
Perona-Wright, G., Jenkins, S. J. and Macdonald, A. S. (2006). Dendritic cell activation and function in response to Schistosoma mansoni. International Journal for Parasitology 36, 711721.
Petchey, O. L. and Gaston, K. J. (2006). Functional diversity: back to basics and looking forward. Ecology Letters 9, 741758.
Poorter, L., Bongers, L. and Bongers, F. (2006). Architecture of 54 moist-forest tree species: Traits, trade-offs, and functional groups. Ecology 87, 12891301.
Popov, A., Abdullah, Z., Wickenhauser, C., Saric, T., Driesen, J., Hanisch, F. G., Domann, E., Raven, E. L., Dehus, O., Hermann, C., Eggle, D., Debey, S., Chakraborty, T., Kronke, M., Utermohlen, O. and Schultze, J. L. (2006). Indoleamine 2,3-dioxygenase-expressing dendritic cells form suppurative granulomas following Listeria monocytogenes infection. Journal of Clinical Investigation 116, 31603170.
Ramharter, M., Kremsner, P. G., Willheim, M., Winkler, H., Graninger, W. and Winkler, S. (2004). Plasmodium falciparum-specific interleukin-2 and tumor necrosis factor-alpha expressing-T cells are associated with resistance to reinfection and severe malaria in healthy African children. European Cytokine Network 15, 189196.
Reimert, C. A., Fitzsimmons, C. M., Joseph, S., Mwatha, J. K., Jones, F. M., Kimani, G., Hoffmann, K. F., Booth, M., Kabatereine, N. B., Dunne, D. W. and Vennervald, B. J. (2006). Eosinophil activity in Schistosoma mansoni infections in vivo and in vitro in relation to plasma cytokine profile pre- and posttreatment with praziquantel. Clinical and Vaccine Immunology 13, 584593.
Riffault, S., Dubuquoy, C., Castagne, N., Baranowski, E., Charley, B. and Eleouet, J. F. (2006). Replication of Bovine respiratory syncytial virus in murine cells depends on type I interferon-receptor functionality. Journal of General Virology 87, 21452148.
Roberts, M. T. M. (2005). Current understandings on the immunology of leishmaniasis and recent developments in prevention and treatment. British Medical Bulletin 75–76, 115130.
Roberts-Thomson, I. C., Grove, D. I., Stevens, D. P. and Warren, K. S. (1976). Suppression of giardiasis during intestinal phase of trichinosis in mouse. Gut 17, 953958.
Rockstroh, J. K. (2006). Management of hepatitis C/HIV coinfection. Current Opinion in Infectious Diseases 19, 813.
Rousseau, D., Lefichoux, Y., Stien, X., Suffia, I., Ferrua, B. and Kubar, J. (1997). Progression of visceral leishmaniasis due to Leishmania infantum in BALB/c mice is markedly slowed by prior infection with Trichinella spiralis. Infection and Immunity 65, 49784983.
Santiago, H. C., Pires, M. F. B., Souza, D. G., Roffe, E., Cortes, D. F., Tafuri, W. L., Teixeira, M. M. and Vieira, L. Q. (2006). Platelet activating factor receptor-deficient mice present delayed interferon-gamma upregulation and high susceptibility to Leishmania amazonensis infection. Microbes and Infection 8, 25692577.
Seixas, E. and Ostler, D. (2005). Plasmodium chabaudi chabaudi (AS): Differential cellular responses to infection in resistant and susceptible mice. Experimental Parasitology 110, 394405.
Seoh, J. Y., Khan, M., Park, S. H., Park, H. K., Shin, M. H., Ha, E. H., Lee, B. E., Yoo, K., Han, H. S., Oh, S., Wi, J. H., Hong, C. K., Oh, C. H., Kim, Y. A. and Park, J. W. (2003). Serum cytokine profiles in patients with Plasmodium vivax malaria: A comparison between those who presented with and without hyperpyrexia. American Journal of Tropical Medicine and Hygiene 68, 102106.
Sharma, S. K., Farah, D., Misra-Bhattacharya, S., Bajpai, P., Agarwal, A. and Mohammad, O. (2006). Escheriosome entrapped soluble blood stage antigens impart protective immunity against a multi-drug resistant isolate of Plasmodium yoelii nigeriensis in BALB/c mice. Vaccine 24, 948956.
Shumilla, J. A., Lacaille, V., Hornell, T. M. C., Huang, J., Narasimhan, S., Relman, D. A. and Mellins, E. D. (2004). Bordetella pertussis infection of primary human monocytes alters HLA-DR expression. Infection and Immunity 72, 14501462.
Singer, S. M. and Nash, T. E. (2000). T-cell-dependent control of acute Giardia lamblia infections in mice. Infection and Immunity 68, 170175.
Sousa-Pereira, S. R., Teixeira, A. L., Silva, L. C. S., Souza, A. L. S., Antunes, C. M., Teixeira, M. M. and Lambertucci, J. R. (2006). Serum and cerebral spinal fluid levels of chemokines and Th2 cytokines in Schistosoma mansoni myeloradiculopathy. Parasite Immunology 28, 473478.
Souza, V. M. O., Jacysyn, J. F. and Macedo, M. S. (2004). IL-4 and IL-10 are essential for immunosuppression induced by high molecular weight proteins from Ascaris suum. Cytokine 28, 92100.
Stadecker, M. J., Asahi, H., Finger, E., Hernandez, H. J., Rutitzky, L. I. and Sun, J. (2004). The immunobiology of Th1 polarization in high-pathology schistosomiasis. Immunological Reviews 201, 168179.
Stebbing, J., Waters, L., Mandalia, S., Bower, M., Nelson, M. and Gazzard, B. (2005). Hepatitis C virus infection in HIV type 1-infected individuals does not accelerate a decrease in the CD4(+) cell count but does increase the likelihood of AIDS-defining events. Clinical Infectious Diseases 41, 906911.
Stevens, D. A. (2006). Th1/Th2 in aspergillosis. Medical Mycology 44, S229S235.
Stewart, M. J., Kulkarni, S. B., Meusel, T. R. and Imani, F. (2006). c-Jun N-terminal kinase negatively regulates dsRNA and RSV induction of tumor necrosis factor-alpha transcription in human epithelial cells. Journal of Interferon and Cytokine Research 26, 521533.
Storkey, J. (2006). A functional group approach to the management of UK arable weeds to support biological diversity. Weed Research 46, 513522.
Sullivan, P. S., Hanson, D. L., Teshale, E. H., Wotring, L. L. and Brooks, J. T. (2006). Effect of hepatitis C infection on progression of HIV disease and early response to initial antiretroviral therapy. Aids 20, 11711179.
Taylor, M. D., Betts, C. J. and Else, K. J. (2000). Peripheral cytokine responses to Trichuris muris reflect those occurring locally at the site of infection. Infection and Immunity 68, 18151819.
Thom, M. L., Hope, J. C., Mcaulay, M., Villarreal-Ramos, B., Coffey, T. J., Stephens, S., Vordermeier, H. M. and Howard, C. J. (2006). The effect of tuberculin testing on the development of cell-mediated immune responses during mycobacterium bovis infection. Veterinary Immunology and Immunopathology 114, 2536.
Tishon, A., Lewicki, H., Andaya, A., Mcgavern, D., Martin, L. and Oldstone, M. B. A. (2006). CD4 T cell control primary measles virus infection of the CNS: Regulation is dependent on combined activity with either CD8 T cells or with B cells: CD4, CD8 or B cells alone are ineffective. Virology 347, 234245.
Torres, D., Janot, L., Quesniaux, V. F. J., Grivennikov, S. I., Maillet, I., Sedgwick, J. D., Ryffel, B. and Erard, F. (2005). Membrane tumor necrosis factor confers partial protection to Listeria infection. American Journal of Pathology 167, 16771687.
Turner, J. D., Faulkner, H., Kamgno, J., Cormont, F., Van Snick, J., Else, K. J., Grencis, R. K., Behnke, J. M., Boussinesq, M. and Bradley, J. E. (2003). Th2 cytokines are associated with reduced worm burdens in a human intestinal helminth infection. Journal of Infectious Diseases 188, 17681775.
Vallance, B. A., Matthaei, K. I., Sanovic, S., Young, I. G. and Collins, S. M. (2000). Interleukin-5 deficient mice exhibit impaired host defence against challenge Trichinella spiralis infections. Parasite Immunology 22, 487492.
Vancott, J. L., Prada, A. E., Mcneal, M. M., Stone, S. C., Basu, M., Huffer, B., Smiley, K. L., Shao, M. Y., Bean, J. A., Clements, J. D., Choi, A. H. C. and Ward, R. L. (2006). Mice develop effective but delayed protective immune responses when immunized as neonates either intranasally with nonliving VP6/LT(R192G) or orally with live rhesus rotavirus vaccine candidates. Journal of Virology 80, 49494961.
von Allmen, N., Christen, S., Forster, U., Gottstein, B., Welle, M. and Muller, N. (2006). Acute trichinellosis increases susceptibility to Giardia lamblia infection in the mouse model. Parasitology 133, 139149.
Walzl, G., Tafuro, S., Moss, P., Openshaw, P. J. M. and Hussell, T. (2000). Influenza virus lung infection protects from respiratory syncytial virus-induced immunopathology. Journal of Experimental Medicine 192, 13171326.
Wang, H. W., Peters, N. and Schwarze, J. (2006). Plasmacytoid dendritic cells limit viral replication, pulmonary inflammation, and airway hyperresponsiveness in respiratory syncytial virus infection. Journal of Immunology 177, 62636270.
Wardle, D. A. and Zackrisson, O. (2005). Effects of species and functional group loss on island ecosystem properties. Nature 435, 806810.
Warrender, C., Forrest, S. and Koster, F. (2006). Modeling intercellular interactions in early Mycobacterium infection. Bulletin of Mathematical Biology 68, 22332261.
Weller, A. F., Harris, A. J. and Ware, J. A. (2006). Artificial neural networks as potential classification tools for dinoflagellate cyst images: A case using the self-organizing map clustering algorithm. Review of Palaeobotany and Palynology 141, 287302.
Werling, D., Howard, C. J., Niederer, E., Straub, O. C., Saalmuller, A. and Langhans, W. (1998). Analysis of the phenotype and phagocytic activity of monocytes/macrophages from cattle infected with the bovine leukaemia virus. Veterinary Immunology and Immunopathology 62, 185195.
Wieland, C. W., Florquin, S., Pater, J. M., Weijer, S. and Van Der Poll, T. (2006). Interleukin-1 contributes to an effective clearance of Mycobacterium kansasii from the respiratory tract. Microbes and Infection 8, 24092413.
Xu, J., Yang, Y., Sun, J., Ding, Y., Su, L., Shao, C. and Jiang, B. (2006). Expression of Toll-like receptors and their association with cytokine responses in peripheral blood mononuclear cells of children with acute rotavirus diarrhoea. Clinical and Experimental Immunology 144, 376381.
Yanagi, Y., Takeda, M. and Ohno, S. (2006). Measles virus: cellular receptors, tropism and pathogenesis. Journal of General Virology 87, 27672779.
Zarantonelli, M. L., Huerre, M., Taha, M. K. and Alonso, J. M. (2006). Differential role of lipooligosaccharide of Neisseria meningitidis in virulence and inflammatory response during respiratory infection in mice. Infection and Immunity 74, 55065512.


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Functional group/guild modelling of inter-specific pathogen interactions: A potential tool for predicting the consequences of co-infection

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