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Concomitant Infections, Parasites and Immune Responses

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Concomitant Infections, Parasites and Immune Responses S23 Concomitant infections, parasites and immune responses F. E. G. COX* Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK Concomitant infections are common in nature and often involve parasites. A number of examples of the interactions between protozoa and viruses, protozoa and bacteria, protozoa and other protozoa, protozoa and helminths, helminths and viruses, helminths and bacteria, and helminths and other helminths are described. In mixed infections the burden of one or both the infectious agents may be increased, one or both may be suppressed or one may be increased and the other suppressed. It is now possible to explain many of these interactions in terms of the effects parasites have on the immune system, particularly parasite-induced immunodepression, and the effects of cytokines controlling polarization to the Th" or Th# arms of the immune response. In addition, parasites may be affected, directly or indirectly, by cytokines and other immune effector molecules and parasites may themselves produce factors that affect the cells of the immune system. Parasites are, therefore, affected when they themselves, or other organisms, interact with the immune response and, in particular, the cytokine network. The importance of such interactions is discussed in relation to clinical disease and the development and use of vaccines. Key words: Concomitant infections, cytokines, protozoa, helminths, bacteria, viruses. field workers and other parasitologists seldom con- sider more than the single organism that directly The term concomitant infections, alternatively called concerns them. The standard parasitological text mixed infections, traditionally refers to a situation in books are silent on this subject and there is virtually which two or more infectious agents coexist in the nothing about concomitant infections in the more same host. In the light of modern concepts of biology specialized texts on epidemiology (Anderson & May, this definition is insufficiently precise and the 1991; Grenfell & Dobson, 1995; Isham & Medley, definition that will be used here is one in which the 1996), parasitism and host behaviour (Barnard & two (or more) concomitant infectious agents are Behnke, 1990; Beckage, 1997), helminth infections specifically designated as being genetically different. and nutrition (Stephenson, 1987), evolution (Brooks This definition permits the inclusion of agents & McLennan, 1993), immunology (Wakelin, 1996) belonging to different species, the commonly ac- or even host-parasite relationships (Toft, cepted view of concomitant infections, and members Aeschlimann & Bolis, 1991). There is some tan- of the same species that are genetically different, for gential reference to hormonal changes induced by example those belonging to a different strain or parasites and possible effects on other parasites by population. In nature, concomitant infections are the Hillgarth & Wingfield (1995) but this is not pursued rule and this has been recognized since the earliest in any depth. There is, therefore, a major gulf recorded times; for example, multiple infections of between the well defined world of text book helminth eggs have been detected in human parasitology, with everything laid out in neat self- coprolites and other human remains from pre- contained sections, and the nicely controlled con- historic sites (see Brothwell & Sandison, 1967; ditions that exist in a laboratory, where there is Cockburn, Cockburn & Reyman, 1998). What is less usually a one to one parasite-host relationship, and well known is that there are numerous interactions, the real world in the field where there may be many both gross and subtle, between different kinds of infections interacting with one another. There are organisms. This fact has been long recognized by many examples of concomitant infections in humans experimental scientists, including parasitologists, and animals (see for example Christensen et al. 1987; who go to great lengths to use animals that are germ Ashford, 1991; Petney & Andrews, 1998; Viera et al. free, specific pathogen free (SPF) or harbour a 1998). The infectious agents concerned may be those known fauna or flora (gnotobiotic). Despite the of the same species, related species or distantly widespread acceptance that different organisms related species. Among the best known examples of commonly occurring together in the same hosts can, the interactions between parasites of the same species and do, influence one another directly or indirectly, are the schistosomes where the presence of an ongoing infection of adult worms inhibits the * Tel: j44 020 7927 2333, Fax: j44 020 7580 9075. establishment of a subsequent infection by larval E-mail: f.cox!lshtm.ac.uk forms, a phenomenon known as concomitant im- Parasitology (2001), 122, S23–S38. " 2001 Cambridge University Press DOI: 10.1017\S003118200001698X Printed in the United Kingdom F. E. G. Cox S24 munity (Smithers, Terry & Hockley, 1969). This immune response. The key cells are the Th (T phenomenon is also seen in other helminth helper) lymphocytes. At first these cells are un- infections, for example, cestodes (see Heath, 1995). committed but they gradually differentiate into Th" In malaria, an ongoing infection is thought by many and Th# cells, each characterized by the cytokines workers not only to induce, but also to be necessary they produce, until eventually they become fully for immunity to a superimposed infection of differentiated and, when this happens, they are parasites with the same or different genotype, a mutually exclusive. The Th" cells produce T" phenomenon called premunition (Sergent, 1937; cytokines, particularly IL-2 that drives the immune Smith et al. 1999). Well known examples of response towards the production of cytotoxic T (Tc) interactions between more distantly related cells and IFN-γ that drives the immune response organisms are those that exist between the Epstein towards the activation of macrophages. Th# cells, on Barr virus and malaria parasites (Burkitt, 1969) and the other hand, produce IL-4, IL-5, IL-10 and IL- between the Human Immunodeficiency Virus (HIV) 13 that lead to the activation of B cells and the and several parasites of which the best known subsequent production of antibody, and to the examples are Cryptosporidium and Leishmania spp. proliferation and differentiation of eosinophils. In (see Ambroise-Thomas, this supplement). shorthand, the Th" responses represent the cell- One of the reasons why so little attention has been mediated arm of the immune response and the Th# paid to concomitant infections is that the interactions responses represent the humoral arm. For further involved are complex and difficult to understand. information, there is an excellent account of this Briefly, such interactions can either be ecological, in subject in Klein & Hor) ejs) ı! (1997). Tc cells are ideally which case the rules of ecology, particularly com- suited for the destruction of virus-infected cells, petition for space or resources, apply or immuno- IFN-γ-activated macrophages are involved in the logical where the rules immunology apply. Anderson killing of intracellular pathogens and the antibody (1994) has stated, in another context, that ‘the produced by B cells is most effective against interaction between the variables that determine the extracellular pathogens such as helminths. The role typical course of infection in an individual patient of Th" and Th# cells in a number of infectious and those that determine the typical course of diseases is well discussed in the various contributions infection in communities of people is often complex in Romagnani (1996) and, with particular relevance and very non-linear in form’. Everything that is said to helminths, by Pritchard, Hewitt & Moqbel (1997). and implied here is made even more complex in the Parasites are no different from other pathogens in case of mixed infections. A number of ecologists, that they inevitably induce some kind of immune particularly those working with helminths, have response except that Tc cells are less involved in begun to appreciate and take cognizance of mixed parasitic infections than in viral infections (see Cox infections and their implications and a considerable & Wakelin, 1998 and Wakelin, 1996 for general amount of progress has been made in this area accounts of the immune responses to parasites). In (Dobson, 1985, 1990; Poulin, 1998) and some of general, it is widely accepted that protective Th" these aspects will be discussed further in this supple- responses predominate in infections caused by ment by Dobson, Poulin, and Kennedy. However, protozoa whereas Th# responses are more important the more subtle interactions that occur in hosts in immunity to helminth infections. In addition, the co-infected with more than one infectious agent, mutual exclusivity mentioned above frequently particularly those involving immunological re- results in extreme polarization in which one arm sponses, have been less well investigated and this is of the immune response is protective and the the area that will be considered in this article. other counter protective. However, these are generalisations and the details of each individual immune response can differ from time to time or from stage to stage of an infection (Allen & Maizels, It is a truism that a host harbouring any infectious 1997). agent is not the same as one that is not infected. The polarization of T cells towards cell-mediated Furthermore, hosts harbouring large
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