Acquired immune heterogeneity and its sources in human helminth infection
Identifieur interne : 004B63 ( Pmc/Corpus ); précédent : 004B62; suivant : 004B64Acquired immune heterogeneity and its sources in human helminth infection
Auteurs : C. D. Bourke ; R. M. Maizels ; F. MutapiSource :
- Parasitology [ 0031-1820 ] ; 2010.
Abstract
Similarities in the immunobiology of different parasitic worm infections indicate that co-evolution of humans and helminths has shaped a common anti-helminth immune response. However, recent
Url:
DOI: 10.1017/S0031182010001216
PubMed: 20946693
PubMed Central: 3021922
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PMC:3021922Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Acquired immune heterogeneity and its sources in human helminth infection</title><author><name sortKey="Bourke, C D" sort="Bourke, C D" uniqKey="Bourke C" first="C. D." last="Bourke">C. D. Bourke</name><affiliation><nlm:aff id="aff1">Institute of Immunology and Infection Research, University of Edinburgh, Ashworth Laboratories, West Mains Road, EH9 3JT</nlm:aff></affiliation></author><author><name sortKey="Maizels, R M" sort="Maizels, R M" uniqKey="Maizels R" first="R. M." last="Maizels">R. M. Maizels</name><affiliation><nlm:aff id="aff1">Institute of Immunology and Infection Research, University of Edinburgh, Ashworth Laboratories, West Mains Road, EH9 3JT</nlm:aff></affiliation></author><author><name sortKey="Mutapi, F" sort="Mutapi, F" uniqKey="Mutapi F" first="F." last="Mutapi">F. Mutapi</name><affiliation><nlm:aff id="aff1">Institute of Immunology and Infection Research, University of Edinburgh, Ashworth Laboratories, West Mains Road, EH9 3JT</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">20946693</idno><idno type="pmc">3021922</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3021922</idno><idno type="RBID">PMC:3021922</idno><idno type="doi">10.1017/S0031182010001216</idno><date when="2010">2010</date><idno type="wicri:Area/Pmc/Corpus">004B63</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">004B63</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Acquired immune heterogeneity and its sources in human helminth infection</title><author><name sortKey="Bourke, C D" sort="Bourke, C D" uniqKey="Bourke C" first="C. D." last="Bourke">C. D. Bourke</name><affiliation><nlm:aff id="aff1">Institute of Immunology and Infection Research, University of Edinburgh, Ashworth Laboratories, West Mains Road, EH9 3JT</nlm:aff></affiliation></author><author><name sortKey="Maizels, R M" sort="Maizels, R M" uniqKey="Maizels R" first="R. M." last="Maizels">R. M. Maizels</name><affiliation><nlm:aff id="aff1">Institute of Immunology and Infection Research, University of Edinburgh, Ashworth Laboratories, West Mains Road, EH9 3JT</nlm:aff></affiliation></author><author><name sortKey="Mutapi, F" sort="Mutapi, F" uniqKey="Mutapi F" first="F." last="Mutapi">F. Mutapi</name><affiliation><nlm:aff id="aff1">Institute of Immunology and Infection Research, University of Edinburgh, Ashworth Laboratories, West Mains Road, EH9 3JT</nlm:aff></affiliation></author></analytic><series><title level="j">Parasitology</title><idno type="ISSN">0031-1820</idno><idno type="eISSN">1469-8161</idno><imprint><date when="2010">2010</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>SUMMARY</title><p>Similarities in the immunobiology of different parasitic worm infections indicate that co-evolution of humans and helminths has shaped a common anti-helminth immune response. However, recent <italic>in vitro</italic> and immuno-epidemiological studies highlight fundamental differences and plasticity within host-helminth interactions. The ‘trade-off’ between immunity and immunopathology inherent in host immune responses occurs on a background of genetic polymorphism, variable exposure patterns and infection history. For the parasite, variation in life-cycle and antigen expression can influence the effector responses directed against them. This is particularly apparent when comparing gastrointestinal and tissue-dwelling helminths. Furthermore, insights into the impact of anti-helminthic treatment and co-infection on acquired immunity suggest that immune heterogeneity arises not from hosts and parasites in isolation, but also from the environment in which immune responses develop. Large-scale differences observed in the epidemiology of human helminthiases are a product of complex host-parasite-environment interactions which, given potential for exposure to parasite antigens <italic>in utero</italic>, can arise even before a parasite interacts with its human host. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Parasitology</journal-id><journal-id journal-id-type="publisher-id">PAR</journal-id><journal-title-group><journal-title>Parasitology</journal-title></journal-title-group><issn pub-type="ppub">0031-1820</issn><issn pub-type="epub">1469-8161</issn><publisher><publisher-name>Cambridge University Press</publisher-name><publisher-loc>Cambridge, UK</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">20946693</article-id><article-id pub-id-type="pmc">3021922</article-id><article-id pub-id-type="doi">10.1017/S0031182010001216</article-id><article-id pub-id-type="pii">S0031182010001216</article-id><article-id pub-id-type="publisher-id">00121</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review Article</subject></subj-group></article-categories><title-group><article-title>Acquired immune heterogeneity and its sources in human helminth infection</article-title><alt-title alt-title-type="left-running">C. D. Bourke and others</alt-title><alt-title alt-title-type="right-running">Heterogeneity in human helminth immunobiology</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>BOURKE</surname><given-names>C. D.</given-names></name><xref ref-type="aff" rid="aff1"></xref><xref ref-type="corresp" rid="cor1">*</xref></contrib><contrib contrib-type="author"><name><surname>MAIZELS</surname><given-names>R. M.</given-names></name><xref ref-type="aff" rid="aff1"></xref></contrib><contrib contrib-type="author"><name><surname>MUTAPI</surname><given-names>F.</given-names></name><xref ref-type="aff" rid="aff1"></xref></contrib></contrib-group><aff id="aff1">Institute of Immunology and Infection Research, University of Edinburgh, Ashworth Laboratories, West Mains Road, EH9 3JT</aff><author-notes><corresp id="cor1"><label>*</label>Corresponding author: Institute of Immunology and Infection Research, University of Edinburgh, Ashworth Laboratories, West Mains Road, Edinburgh, EH9 3JT. Tel: +44 (0)131 6505445. E-mail: <email xlink:href="C.D.Bourke@sms.ed.ac.uk">C.D.Bourke@sms.ed.ac.uk</email></corresp></author-notes><pub-date pub-type="ppub"><month>2</month><year>2011</year></pub-date><pub-date pub-type="epub"><day>15</day><month>10</month><year>2010</year></pub-date><volume>138</volume><issue>2</issue><fpage>139</fpage><lpage>159</lpage><history><date date-type="received"><day>12</day><month>7</month><year>2010</year></date><date date-type="rev-recd"><day>18</day><month>7</month><year>2010</year></date><date date-type="accepted"><day>18</day><month>7</month><year>2010</year></date></history><permissions><copyright-statement>Copyright © Cambridge University Press 2010 The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution-NonCommercial-ShareAlike licence <copyright-year>2010</copyright-year><copyright-holder>Cambridge University Press</copyright-holder><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-sa/2.5/"><license-p>The online version of this article is published within an Open Access environment subject to the conditions of the Creative Commons Attribution-NonCommercial-ShareAlike licence </license></permissions><self-uri xlink:title="pdf" xlink:type="simple" xlink:href="S0031182010001216a.pdf"></self-uri><abstract><title>SUMMARY</title><p>Similarities in the immunobiology of different parasitic worm infections indicate that co-evolution of humans and helminths has shaped a common anti-helminth immune response. However, recent <italic>in vitro</italic> and immuno-epidemiological studies highlight fundamental differences and plasticity within host-helminth interactions. The ‘trade-off’ between immunity and immunopathology inherent in host immune responses occurs on a background of genetic polymorphism, variable exposure patterns and infection history. For the parasite, variation in life-cycle and antigen expression can influence the effector responses directed against them. This is particularly apparent when comparing gastrointestinal and tissue-dwelling helminths. Furthermore, insights into the impact of anti-helminthic treatment and co-infection on acquired immunity suggest that immune heterogeneity arises not from hosts and parasites in isolation, but also from the environment in which immune responses develop. Large-scale differences observed in the epidemiology of human helminthiases are a product of complex host-parasite-environment interactions which, given potential for exposure to parasite antigens <italic>in utero</italic>, can arise even before a parasite interacts with its human host. This review summarizes key differences identified in human acquired immune responses to nematode and trematode infections of public health importance and explores the factors contributing to these variations.</p></abstract><kwd-group kwd-group-type=""><title>Key words</title><kwd>heterogeneity</kwd><kwd>helminth</kwd><kwd>human</kwd><kwd>nematode</kwd><kwd>trematode</kwd><kwd>schistosome</kwd><kwd>immune response</kwd></kwd-group><counts><page-count count="21"></page-count></counts></article-meta></front><body><sec sec-type="intro" id="sec1"><title>INTRODUCTION</title><p>Over a third of the human population is currently infected by one or more species of parasitic helminth (Hotez <italic>et al.</italic> <xref ref-type="bibr" rid="ref70">2008</xref>). Chronically-infected hosts must strike a balance between anti-parasite protective responses and limiting immune-mediated pathology (Hoffmann <italic>et al.</italic> <xref ref-type="bibr" rid="ref69">2002</xref>), whilst parasites have developed strategies to prolong intra-host survival and fecundity. Throughout their co-evolutionary history these forces, as often in concert as in opposition, have driven diversity in both parasites (Maizels <italic>et al.</italic> <xref ref-type="bibr" rid="ref96">2001</xref>) and the genetics of the host immune response (Fumagalli <italic>et al.</italic> <xref ref-type="bibr" rid="ref53">2009</xref>; Maizels, <xref ref-type="bibr" rid="ref94">2009</xref>), the latter especially evident in the human population. Experimental models are invaluable in mechanistic studies of helminth-induced immune responses <italic>in vivo</italic>; however, reductionist laboratory models inevitably seek to minimize variation in the host, the context of infection and polymorphism in the parasite itself. Moreover, integral differences in the immune systems of different host species (Mestas and Hughes, <xref ref-type="bibr" rid="ref105">2004</xref>) and the inability of many anthropophilic helminths to naturally infect laboratory animals mean that current experimental models do not reflect the complexity of human helminth immunobiology. Most importantly, models cannot easily replicate the major sources of human immune heterogeneity such as parasite transmission dynamics (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref115">1997</xref>), distribution of intermediate hosts (Gryseels <italic>et al.</italic> <xref ref-type="bibr" rid="ref60">2006</xref>), distinct intra-population exposure patterns (Rudge <italic>et al.</italic> <xref ref-type="bibr" rid="ref134">2008</xref>), therapeutic interventions (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref111">2005</xref>) and concurrent or previous infections with other pathogen species (Correa-Oliveira <italic>et al.</italic> <xref ref-type="bibr" rid="ref22">2002</xref>).</p><p>This review highlights differences in the human acquired immune response to a variety of nematode and trematode infections of public health importance and explores some of the factors contributing to these variations, particularly differences arising from helminth life-history traits.</p></sec><sec id="sec2"><title>COMMON FEATURES OF THE ACQUIRED IMMUNE RESPONSE</title><p>The most prevalent human helminthiases are caused by nematode species including filarial worms (<italic>Brugia malayi, Onchocerca volvulus</italic> and <italic>Wuchereria bancrofti</italic>) and soil-transmitted helminths (Hotez <italic>et al.</italic> <xref ref-type="bibr" rid="ref70">2008</xref>): <italic>Ascaris lumbricoides, Trichuris trichiura</italic>, hookworm (<italic>Ancyclostoma duodenale</italic> and <italic>Necator americanus</italic>), <italic>Strongyloides</italic> spp., and <italic>Enterobius vermicularis</italic>. Of the trematodes, <italic>Schistosoma</italic> spp. are of greatest public health importance, with the 3 predominant species (<italic>S. haematobium, S. japonicum</italic> and <italic>S. mansoni</italic>) accounting for over 200 million current infections worldwide (Gryseels <italic>et al.</italic> <xref ref-type="bibr" rid="ref60">2006</xref>). In addition, and beyond the scope of this article, there are many important human cestode parasites which have been expertly discussed elsewhere (Zhang <italic>et al.</italic> <xref ref-type="bibr" rid="ref170">2008</xref>).</p><p>The principal cellular mediators of human-helminth interactions are CD4<sup>+</sup> T cells, which can differentiate into alternative lineages once activated; Th1, Th2, Th17 and T regulatory (Treg), as summarized in <xref ref-type="fig" rid="fig01">Fig. 1</xref>. Selective differentiation is first driven by innate antigen-presenting cells (APC) but, as responses mature during the course of chronic infection, cytokine-mediated cross-regulation between T cell subsets becomes increasingly important. Differences in acquired immune responses to helminth infection can arise via heterogeneity in how parasites initially interact with host cells, polarize local and systemic responses and/or modulate effector responses in chronic infection. There are two principal immunological features believed to be common amongst helminth infections. (1) Polarization of CD4<sup>+</sup> T cells towards a Th2 phenotype. In humans, this phenotype is associated with production of interleukins (IL-)4, 5, 9, 10 and 13 (Turner <italic>et al.</italic> <xref ref-type="bibr" rid="ref155">2003</xref>; Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref74">2004<italic>b</italic></xref>; Quinnell <italic>et al.</italic> <xref ref-type="bibr" rid="ref130">2004</xref>), secretion of IgE and IgG4 isotypes by plasma cells (Hagan <italic>et al.</italic> <xref ref-type="bibr" rid="ref61">1991</xref>) and activation of downstream effector cells such as eosinophils (reviewed by (Klion and Nutman, <xref ref-type="bibr" rid="ref84">2004</xref>)). (2) Immunosuppression of both worm-specific and generalized immune responses. Inducible mechanisms include secretion of suppressive cytokines, such as IL-10 and TGF-<italic>β</italic>, and expansion of regulatory cell populations, particularly Tregs (Doetze <italic>et al.</italic> <xref ref-type="bibr" rid="ref36">2000</xref>; Watanabe <italic>et al.</italic> <xref ref-type="bibr" rid="ref160">2007</xref>; Babu <italic>et al.</italic> <xref ref-type="bibr" rid="ref4">2009</xref>). The progression of host responses from effector Th2 to a so-called ‘modified Th2’ phenotype associated with elevated levels of Treg-associated molecules and reduced Th2 effector cytokine responses (Maizels and Yazdanbakhsh, <xref ref-type="bibr" rid="ref99">2003</xref>), suggests that both features play a functional, and potentially cross-regulatory, role in helminth immunobiology.
<fig id="fig01" position="float"><label>Fig. 1</label><caption><p>Summary of the major CD4+ T cell differentiation pathways following activation in the periphery. Cytokines and transcription factors involved in T cell polarization are shown in boxes and within cells respectively. Effector cell types and cytokines associated with each CD4+ T cell phenotype are given adjacent to relevant cells. Th0 – naïve T cell, * ROR<italic>γ</italic>t – murine transcription factor, the human orthologue is RORC2. Figure adapted from Deenick and Tangyne (<xref ref-type="bibr" rid="ref30">2007</xref>) and Diaz and Allen (<xref ref-type="bibr" rid="ref35">2007</xref>).</p></caption><graphic xlink:href="S0031182010001216_fig1"></graphic></fig></p><p>Despite similarities in the immune responses elicited by different helminths, immunological studies often yield contradictory results in different human populations and different species of helminth infection, which are discussed below. To an extent this is unsurprising as expanding research into human helminthiases has inevitably led to a greater appreciation of the intricacies of their immunobiology. The discovery of new cell populations including Treg and Th17 and the more recent description of IL-5 and IL-9 producing CD4+ T cells, which differentiate from Th2 cells in an IL-33 or TGF-<italic>β</italic>/IL-4-dependent manner respectively, has led to a re-evaluation of the classical Th1-Th2 paradigm (Dardalhon <italic>et al.</italic> <xref ref-type="bibr" rid="ref26">2008</xref>; Kurowska-Stolarska <italic>et al.</italic> <xref ref-type="bibr" rid="ref86">2008</xref>; Veldhoen <italic>et al.</italic> <xref ref-type="bibr" rid="ref156">2008</xref>). Furthermore the CD4+ T cell axis can be regulated both by effector cytokines from CD4+ T cell populations themselves (IFN<italic>γ</italic>, IL-4 and IL-21 (Wilson <italic>et al.</italic> <xref ref-type="bibr" rid="ref165">2008</xref>; Babu <italic>et al.</italic> <xref ref-type="bibr" rid="ref4">2009</xref>)) and innate and adaptive non-T cell populations, which both present antigen to activate T cells and contribute significant levels of these same cytokines. Helminth-induced alternatively activated macrophages exhibit particular plasticity in this respect (Jenkins and Allen, <xref ref-type="bibr" rid="ref76">2010</xref>). Studies showing that Th2 IL-4 and IL-5 responses can be dissociated in human nematode (Sartono <italic>et al.</italic> <xref ref-type="bibr" rid="ref135">1997</xref>) and trematode (Scott <italic>et al.</italic> <xref ref-type="bibr" rid="ref138">2000</xref>) infections indicate that even established immune phenotypes involve heterogeneous effector responses to helminth infection. As more data become available on human anti-helminth responses, particularly in terms of the more recently described cytokines (e.g. IL-17, IL-21, IL-23, IL-33), comparative studies between helminth groups will be better able to identify similarities and differences in these responses.</p></sec><sec id="sec3"><title>HETEROGENEITY IN PROTECTIVE IMMUNE RESPONSES</title><p>Protective immunity in human helminthiases encompasses a range of overlapping mechanisms: (a) complete elimination of parasites (sterile immunity), (b) resistance to <italic>de novo</italic> infection (non-sterile immunity, also called ‘concomitant immunity’) and (c) reduction of immunopathology (tolerance). The former two processes can be grouped as anti-parasite immunity, whilst the latter involves immune-mediated regulation of pathological effector responses. The high prevalence of chronic helminth infection in endemic populations suggests that sterile immunity is rarely generated (Hotez <italic>et al.</italic> <xref ref-type="bibr" rid="ref70">2008</xref>). However, the decline in infection intensity at an earlier age in populations with high infection intensity (Woolhouse, <xref ref-type="bibr" rid="ref166">1998</xref>) and more rapid development of resistance to re-infection post-treatment in individuals with long-term exposure to infection (Black <italic>et al.</italic> <xref ref-type="bibr" rid="ref8">2010</xref>) indicates that non-sterile immunity, though slow to develop, does occur with cumulative exposure. Conversely, since the majority of helminth infections are asymptomatic, it is clear that tolerance of low-level infection can be readily elicited to limit immunopathology (Dessein <italic>et al.</italic> <xref ref-type="bibr" rid="ref33">2004</xref>). The balance between anti-parasite and anti-pathology responses is inevitably shaped by the specific immunopathogenesis of different helminth species. Contrary to phylogenetic distinctions between nematodes and trematodes, one of the main functional delineations between helminth infections is that between species where adult worms reside in the gastrointestinal (GI) tract and those that inhabit host tissues.</p><sec id="sec3-1"><title>Anti-parasite immune responses</title><p>Expulsion of GI nematodes is dependent on highly polarised Th2 responses (reviewed by (Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref72">2009</xref>; Jenkins and Allen, <xref ref-type="bibr" rid="ref76">2010</xref>)) and elevated titres of systemic and parasite-specific Th2 cytokines are negatively associated with infection intensity in untreated populations (Turner <italic>et al.</italic> <xref ref-type="bibr" rid="ref155">2003</xref>). Th2-induced smooth muscle hypercontractility and mucus secretion by goblet cells are known to facilitate clearance of murine GI nematode infections (Finkelman <italic>et al.</italic> <xref ref-type="bibr" rid="ref47">2004</xref>), but these physical means of worm expulsion are absent in the tissues. The immunological relevance of these differences has not been tested in humans.</p><p>Resistance to re-infection by GI nematodes post-treatment also tends to be unequivocally Th2-mediated (Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref73">2004<italic>a</italic></xref>,<xref ref-type="bibr" rid="ref74"><italic>b</italic></xref>; Quinnell <italic>et al.</italic> <xref ref-type="bibr" rid="ref130">2004</xref>). Post-treatment resistance to hookworm and <italic>T. trichiura</italic> infection is associated with pre-treatment levels of IL-5 (Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref73">2004<italic>a</italic></xref>; Quinnell <italic>et al.</italic> <xref ref-type="bibr" rid="ref130">2004</xref>) and negative associations have also been shown between IL-5/IL-13 and re-infection with <italic>A. lumbricoides</italic> and <italic>T. trichiura</italic> (Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref74">2004<italic>b</italic></xref>). However, even between GI nematode species the relationship between Th2 cytokines and resistance to re-infection has been shown to vary according to parasite life-history. For example despite multiple shared risk factors for co-infection with <italic>A. lumbricoides</italic> and <italic>T. trichiura</italic>, pre-treatment Th2 cytokine titres were only associated with post-treatment resistance to the latter (Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref73">2004<italic>a</italic></xref>). Furthermore, parasite-specific IL-10 was found to be an indicator of species-specific susceptibility, being negatively associated with <italic>T. trichiura</italic> but positively associated with <italic>A. lumbricoides</italic> egg counts (Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref73">2004<italic>a</italic></xref>).</p><p>Th2-type responses are also involved in protective immunity in tissue-dwelling helminths; however, chronically infected individuals tend to mount Th1-Th2 mixed responses (Joseph <italic>et al.</italic> <xref ref-type="bibr" rid="ref79">2004</xref>; Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref116">2007</xref>), thought to be involved in limiting infection intensity (Turaga <italic>et al.</italic> <xref ref-type="bibr" rid="ref154">2000</xref>). In an <italic>O. volvulus</italic>-endemic population in Cameroon, despite a predominant Th2 bias, putative immunity correlated with elevated titres of parasite-specific Th1 (IFN<italic>γ</italic>), Th2 (IL-5) and innate (granulocyte-macrophage colony-stimulating factor (GM-CSF)) effector cytokines (Turaga <italic>et al.</italic> <xref ref-type="bibr" rid="ref154">2000</xref>). Similarly, schistosome-specific IFN<italic>γ</italic> production by peripheral blood mononuclear cells (PBMC) correlates with immunity to schistosomiasis (Viana <italic>et al.</italic> <xref ref-type="bibr" rid="ref158">1994</xref>). Mixed Th1-Th2 cytokine responses are observed in chronic trichuriasis in the gut but have not been significantly associated with infection intensity (Faulkner <italic>et al.</italic> <xref ref-type="bibr" rid="ref45">2002</xref>).</p><p>Antibody-mediated protection from helminths is typically attributed to elevated titres of parasite-specific IgE (Faulkner <italic>et al.</italic> <xref ref-type="bibr" rid="ref45">2002</xref>; Pearce and MacDonald, <xref ref-type="bibr" rid="ref125">2002</xref>), whilst a low IgE:IgG4 is associated with susceptibility to schistosome (Hagan <italic>et al.</italic> <xref ref-type="bibr" rid="ref61">1991</xref>) and GI infections (Figueiredo <italic>et al.</italic> <xref ref-type="bibr" rid="ref46">2010</xref>). However, positive correlations between parasite-specific IgE and other isotypes (Viana <italic>et al.</italic> <xref ref-type="bibr" rid="ref159">1995</xref>) and studies identifying more pronounced associations between infection intensity and non-IgE isotypes (Webster <italic>et al.</italic> <xref ref-type="bibr" rid="ref161">1997</xref>) suggest that there is redundancy in antibody-mediated protective immunity. In addition, given the potentially immunopathogenic outcomes of IgE-mediated cellular effector responses (Nutman and Kumaraswami, <xref ref-type="bibr" rid="ref120">2001</xref>; Cooper <italic>et al.</italic> <xref ref-type="bibr" rid="ref21">2004</xref>), it is unsurprising that propagation of alternate antibody isotypes in chronically infected hosts may be favourable. A variety of studies investigating other antibody isotypes in schistosomiasis provide conflicting evidence for their role in resistance to infection with different species. For example, whilst polyclonal adult worm-specific IgA titres decline with age and infection intensity in <italic>S. haematobium</italic> endemic areas (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref115">1997</xref>), the opposite pattern has been observed for <italic>S. japonicum</italic>-specific IgA in the Philippines (Acosta <italic>et al.</italic> <xref ref-type="bibr" rid="ref1">2004</xref>). Similarly, whilst the former study found that <italic>S. haematobium</italic> adult worm-specific IgG1 increased with age and peaked in individuals with low infection intensity (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref115">1997</xref>), IgG1 titres were significantly positively associated with intensity of <italic>S. mansoni</italic> infection in Brazil (de Jesus <italic>et al.</italic> <xref ref-type="bibr" rid="ref29">2000</xref>) and Kenya (Naus <italic>et al.</italic> <xref ref-type="bibr" rid="ref118">1999</xref>). The role of IgM in anti-schistosome responses is also controversial as adult worm and egg-specific IgM increase with <italic>S. haematobium</italic> and <italic>S. japonicum</italic> infection intensity in some populations (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref115">1997</xref>; Acosta <italic>et al.</italic> <xref ref-type="bibr" rid="ref1">2004</xref>), but adult-worm-specific titres were lowest in individuals patently infected with <italic>S. mansoni</italic> elsewhere (Viana <italic>et al.</italic> <xref ref-type="bibr" rid="ref159">1995</xref>; Caldas <italic>et al.</italic> <xref ref-type="bibr" rid="ref17">2000</xref>). Potential sources of variation in protective immunity within and between schistosome-infected populations are discussed in the following sections.</p><p>For filarial infections larvae-specific antibodies acquired with age have been shown to confer resistance to re-infection post-treatment (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref28">1991<italic>b</italic></xref>); however, the immunogenic epitopes within the larval proteome could not be identified (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref27">1991<italic>a</italic></xref>). Few studies have directly compared schistosome and nematode-specific antibody responses; however, studies to date suggest that differences do exist. <italic>W. bancrofti</italic> microfilaria and circulating antigen negative individuals were found to have the lowest parasite-specific IgG4:IgE (Jaoko <italic>et al.</italic> <xref ref-type="bibr" rid="ref75">2006</xref>) as has been observed in schistosome studies (Hagan <italic>et al.</italic> <xref ref-type="bibr" rid="ref61">1991</xref>). However, unlike in chronic schistosomiasis, the ratios did not differ between communities with high and low intensity infection indicating that relative changes in these isotypes may be less dependent on host exposure history (Jaoko <italic>et al.</italic> <xref ref-type="bibr" rid="ref75">2006</xref>). IgG2 also appears to limit infection intensity when directed against <italic>W. bancrofti</italic> microfilaria (Jaoko <italic>et al.</italic> <xref ref-type="bibr" rid="ref75">2006</xref>), but is ineffective against schistosome larvae (Demeure <italic>et al.</italic> <xref ref-type="bibr" rid="ref32">1993</xref>).</p><p>The specific target of antibody responses is particularly important for development of protective immunity, although the majority of field studies focus on crude antigen preparations. Early schistosome studies identified isotype-specific antibody responses to different antigen types within the parasite proteome (Langley <italic>et al.</italic> <xref ref-type="bibr" rid="ref88">1994</xref>), but it was not until the advent of mass spectrometric analysis that parasite peptides recognized by different antibody isotypes could be identified within crude preparations (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref111">2005</xref>, <xref ref-type="bibr" rid="ref112">2008</xref>). Relative exposure of immunogenic peptides clearly plays a role in cumulative development of protective antibodies. For example, antibodies against the larval surface are associated with protection against <italic>W. bancrofti</italic> (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref27">1991<italic>a</italic></xref>) and antibodies targeting cryptic antigens released by dying adult worms may influence the course of schistosome infection (Woolhouse and Hagan, <xref ref-type="bibr" rid="ref167">1999</xref>). It remains unclear whether there is a single antibody isotype that uniformly protects against helminth infection and it seems likely that redundancy within host antibody responses, variation between parasite species and/or host populations have all contributed to isotype-specific variations observed in the field.</p></sec><sec id="sec3-2"><title>Anti-pathology immune responses</title><p>Limiting immunopathology in patent helminth infection is a combination of parasite and host-mediated processes that synergize to limit aberrant immune reactivity and damage to the host. This is necessarily a compromise as dampening immune responses to infection also limits their efficacy at clearing infection (Maizels and Yazdanbakhsh, <xref ref-type="bibr" rid="ref99">2003</xref>). For tissue-dwelling helminths close association with host tissues throughout their life-cycle means that effector responses to adult worms and migrating larvae in these loci must be tightly regulated (Montenegro <italic>et al.</italic> <xref ref-type="bibr" rid="ref107">1999</xref>). In chronic schistosomiasis, for example, Th2-polarized responses account for the majority of host pathologies including hepatic fibrosis (Coutinho <italic>et al.</italic> <xref ref-type="bibr" rid="ref24">2007</xref>) and egg-specific responses promote granuloma formation (ElRidi <italic>et al.</italic> <xref ref-type="bibr" rid="ref40">1997</xref>), whilst Th2-mediated damage is mitigated by Th1-type (Henri <italic>et al.</italic> <xref ref-type="bibr" rid="ref66">2002</xref>; Dessein <italic>et al.</italic> <xref ref-type="bibr" rid="ref33">2004</xref>) and innate inflammatory cytokines (TNF<italic>α</italic> and IL-6 (Booth <italic>et al.</italic> <xref ref-type="bibr" rid="ref9">2004<italic>a</italic></xref>; Wilson <italic>et al.</italic> <xref ref-type="bibr" rid="ref165">2008</xref>)). The importance of Tregs in balancing Th1 and Th17 responses in human filarial infections has been recently highlighted by Babu and colleagues who identified a positive correlation between lymphoedema and Th1/Th17 cytokine and Toll-like receptor expression in individuals with low expression of Treg-associated molecules (Babu <italic>et al.</italic> <xref ref-type="bibr" rid="ref4">2009</xref>).</p><p>Ubiquitous exposure to commensal bacteria and food antigens means that antigen-presentation and inflammatory responses are highly regulated in the gut to maintain a physical barrier between the lumen and host tissues (Mayer, <xref ref-type="bibr" rid="ref102">2000</xref>). GI nematodes are also able to actively down-regulate effector responses in the gut to maintain this regulatory environment (reviewed by Maizels and Yazdanbakhsh, <xref ref-type="bibr" rid="ref99">2003</xref>). Both <italic>Ascaris</italic> spp. and <italic>Trichuris</italic> spp. infections are also associated with reduced cellular responsiveness to both non-specific agonists and parasite-specific antigens in humans (Figueiredo <italic>et al.</italic> <xref ref-type="bibr" rid="ref46">2010</xref>). The rebound in <italic>N. americanus</italic>-specific IFN<italic>γ</italic> observed after anti-helminthic treatment to clear infection suggests that Th1 responses may be particularly regulated in chronic hookworm infection (Quinnell <italic>et al.</italic> <xref ref-type="bibr" rid="ref130">2004</xref>).</p><p>However, GI nematodes are not homogeneous in the immune responses that they induce and thus pose distinct immunopathological risks. <italic>T. trichiura</italic> infection induces a mixed Th1-Th2 cytokine profile (Faulkner <italic>et al.</italic> <xref ref-type="bibr" rid="ref45">2002</xref>), whilst <italic>Ascaris lumbricoides</italic> infection leads to a highly Th2 environment (Cooper <italic>et al.</italic> <xref ref-type="bibr" rid="ref20">2000</xref>). It has been postulated that murine <italic>Trichuris</italic> spp. are distinct from other GI infections in specifically up-regulating Th1 cytokines as a means of evading Th2-mediated clearance (refer to review by Else, <xref ref-type="bibr" rid="ref41">2005</xref>); however, fostering a more mixed cytokine response may also limit pathology. IL-10 secretion is highly prevalent in <italic>T. trichiura</italic> endemic populations with 97% of a Cameroonian cohort secreting parasite-specific IL-10 and older individuals producing the highest titres of non-specific IL-10 (Faulkner <italic>et al.</italic> <xref ref-type="bibr" rid="ref45">2002</xref>), suggesting that systemic immunoregulation coincides with cumulative exposure to infection.</p></sec></sec><sec id="sec4"><title>SOURCES OF ACQUIRED IMMUNE HETEROGENEITY</title><sec id="sec4-1"><title>Helminth life history</title><p>Helminths undergo complex life cycles leading to both physical and molecular variations during the course of an infection. <xref ref-type="table" rid="tab01">Table 1</xref> summarizes the key differences in helminth life histories that can introduce heterogeneity in the development of the host immune response to infection. Furthermore, the range of molecules and mechanisms that underlie helminth-mediated immunomodulation have been reviewed elsewhere (Maizels and Yazdanbakhsh, <xref ref-type="bibr" rid="ref99">2003</xref>; Maizels <italic>et al.</italic> <xref ref-type="bibr" rid="ref98">2009</xref>) and present a potential source of immune heterogeneity in themselves.
<table-wrap id="tab01" position="float"><label>Table 1</label><caption><p>Summary of parasite-factors that may influence the host acquired immune response to helminth infection (Anderson and May, <xref ref-type="bibr" rid="ref3">1992</xref>; Maizels <italic>et al</italic>. <xref ref-type="bibr" rid="ref95">1993</xref>; Maizels and Kurniawan-Atmadja, <xref ref-type="bibr" rid="ref97">2002</xref>; Gryseels <italic>et al</italic>. <xref ref-type="bibr" rid="ref60">2006</xref>; Hotez <italic>et al</italic>. <xref ref-type="bibr" rid="ref70">2008</xref>).</p></caption><graphic xlink:href="S0031182010001216_tab1"></graphic><table-wrap-foot><fn id="tfn1_1"><label>*</label><p>All hookworm species.</p></fn><fn id="tfn1_2"><label>**</label><p><italic>Strongyloides stercoralis</italic> only.</p></fn><fn id="tfn1_3"><label>***</label><p>All <italic>S. haematobium, S. japonicum</italic> and <italic>S. mansoni</italic> infections.</p></fn><fn id="tfn1_4"><label>^</label><p>Life-span of <italic>S. mansoni</italic> estimated using maximum likelihood techniques to assess pre- and post-treatment field data (Fulford <italic>et al.</italic> <xref ref-type="bibr" rid="ref52">1995</xref>).</p></fn><fn id="tfn1_5"><p>Abbreviations: <italic>A. lum – Ascaris lumbricoides, E. ver – Enterobis vermicularis, N. ame – Necator americanus, Stro</italic> spp<italic>. – Strongyloides</italic> spp<italic>., T. tri – Trichuris trichiura, B. mal – Brugia malayi, O. vol – Onchocerca volvulus, W. ban – Wuchereria bancrofti, S. hae – Schistosoma haematobium, S. jap – Schistosoma japonicum, S. man – Schistosoma mansoni</italic>, Af – Africa, As – Asia, LAm – Latin America, SEAs – South East Asia, SSAf – Sub-Saharan Africa, <italic>Ano</italic> spp<italic>. – Anopheles</italic> spp<italic>. mosquito, Aed</italic> spp<italic>. – Aedes</italic> spp<italic>. mosquito, Cul</italic> spp<italic>. – Culex</italic> spp<italic>. mosquito, B. gla – Biomphalaria glabrata</italic> (<italic>aquatic snail</italic>), <italic>Bul</italic> spp<italic>. – Bulinus</italic> spp<italic>.</italic> (<italic>aquatic snail</italic>), mf – microfilariae.</p></fn></table-wrap-foot></table-wrap></p></sec><sec id="sec4-2"><title>Parasite transmission route</title><p>Transmission route impacts upon where and how infection is initially detected by the immune system. Immature helminths face site-specific challenges as they invade their host, for example species that are transmitted through the skin tend to suffer immune attrition in this organ (He <italic>et al.</italic> <xref ref-type="bibr" rid="ref65">2005</xref>). Amongst the schistosome species, which invade by active penetration, <italic>S. japonicum</italic> cercariae migrate most rapidly to the dermis and this species also elicits the most pro-inflammatory response in human skin (He <italic>et al.</italic> <xref ref-type="bibr" rid="ref64">2002</xref>). In contrast <italic>S. haematobium</italic> and <italic>S. mansoni</italic> cercariae promote up-regulation of immunoregulatory proteins including IL-10 and IL-1 receptor antagonist (He <italic>et al.</italic> <xref ref-type="bibr" rid="ref64">2002</xref>), highlighting heterogeneity in the effector and regulatory immune mechanisms elicited even by closely-related species.</p><p>Arthropod-borne larvae are also exposed to immune attrition in human cutaneous tissue when they enter during blood-feeding by the vector. However, unlike actively penetrating parasites, antigens, enzymes and immunosuppressive molecules in arthropod saliva may skew the host immune response in favour of vector-transmitted larvae (Demeure <italic>et al.</italic> <xref ref-type="bibr" rid="ref31">2005</xref>). Furthermore, where a single helminth species (such as <italic>W. bancrofti</italic>) can be transmitted by multiple mosquito species of 4 different genera (<italic>Aedes, Anopheles, Culex</italic> and <italic>Mansonia</italic>) (Maizels and Kurniawan-Atmadja, <xref ref-type="bibr" rid="ref97">2002</xref>), there is potential for the human immune response to be differently shaped in each instance. The presence of <italic>Wolbachia</italic> spp. bacterial endosymbionts in mosquito vectors and almost all filarial helminth species has also been suggested to influence host T-cell responsiveness (Brattig, <xref ref-type="bibr" rid="ref13">2004</xref>), but this is yet to be verified.</p><p>On a broader scale transmission route can determine distribution of immune-mediated morbidities within host populations. One example is the lower prevalence of Sowda in <italic>O. volvulus</italic>-infected men relative to women inhabiting the same area, which has been attributed to development of immune tolerance after repeated exposure to <italic>O. volvulus</italic> vectors during agricultural work (Brattig, <xref ref-type="bibr" rid="ref13">2004</xref>; Trpis, <xref ref-type="bibr" rid="ref153">2006</xref>).</p><p>Following initial infection, larval migration may also contribute to immune heterogeneity between GI nematodes, particularly with respect to anti-pathology immunity. Clinical measures of atopic reactivity suggest that hookworm with lung-migratory stages effectively suppress asthma and wheeze in the lung (Scrivener <italic>et al.</italic> <xref ref-type="bibr" rid="ref139">2001</xref>; Leonardi-Bee <italic>et al.</italic> <xref ref-type="bibr" rid="ref90">2006</xref>). Therapeutic <italic>N. americanus</italic> infection is able to dampen inflammation both in the lung and in the gut, where adult worms reside (Falcone and Pritchard, <xref ref-type="bibr" rid="ref43">2005</xref>; Croese <italic>et al.</italic> <xref ref-type="bibr" rid="ref25">2006</xref>). On the other hand, <italic>Trichuris</italic> spp. which inhabit the lower intestine and do not migrate through the lung, can dampen inflammatory pathologies in the gut (Reddy and Fried, <xref ref-type="bibr" rid="ref132">2007</xref>) but are less effective at regulating clinical allergy elsewhere (Bager <italic>et al.</italic> <xref ref-type="bibr" rid="ref5">2010</xref>). Interestingly <italic>A. lumbricoides</italic> infection, which has a lung migratory phase, does not reduce asthmatic responses and is associated with elevated atopy (Flohr <italic>et al.</italic> <xref ref-type="bibr" rid="ref51">2009</xref>). There are many potential reasons for variation in the effect of GI helminth infection on clinical allergy (reviewed elsewhere (Flohr <italic>et al.</italic> <xref ref-type="bibr" rid="ref51">2009</xref>)) and conflicting results in existing literature (Leonardi-Bee <italic>et al.</italic> <xref ref-type="bibr" rid="ref90">2006</xref>) and a lack of studies which directly compare GI nematode infections with distinct migratory pathways make it difficult to conclude on the source of observed variations.</p></sec><sec id="sec4-3"><title>Life-cycle stages</title><p>Chronically infected individuals are simultaneously exposed to 3 helminth life-cycle stages; infective larvae, adult worms and transmission stage parasites (eggs, immature larvae or microfilariae). Both proteomic (Moreno and Geary, <xref ref-type="bibr" rid="ref108">2008</xref>) and DNA micro-array studies (Jolly <italic>et al.</italic> <xref ref-type="bibr" rid="ref78">2007</xref>; Fitzpatrick <italic>et al.</italic> <xref ref-type="bibr" rid="ref49">2009</xref>) have shown that these life-cycle stages are molecularly different and thus elicit stage-specific immune responses that change over time.</p><p>In experimental murine studies where the course of infection can be tracked from its acute phase, there is a clear link between the onset of egg production (week 5–6 post-infection) and a Th1-to-Th2 shift in the cellular response to schistosomiasis (Pearce and MacDonald, <xref ref-type="bibr" rid="ref125">2002</xref>). Although the Th1-to-Th2 shift is less clear in human infections, defined egg peptides can specifically induce Th2 responses in human basophils, DCs and T cells <italic>in vitro</italic> (Schramm <italic>et al.</italic> <xref ref-type="bibr" rid="ref137">2003</xref>; Everts <italic>et al.</italic> <xref ref-type="bibr" rid="ref42">2009</xref>). Th2 polarization by schistosome eggs also induces granuloma formation (ElRidi <italic>et al.</italic> <xref ref-type="bibr" rid="ref40">1997</xref>), which facilitates passage of eggs from venous blood into the gut/bladder and subsequent transmission to the environment (Karanja <italic>et al.</italic> <xref ref-type="bibr" rid="ref81">1997</xref>; Pearce and MacDonald, <xref ref-type="bibr" rid="ref125">2002</xref>). Carbohydrate antigens on the schistosome egg surface also promote IgM secretion, which lacks immunological memory (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref113">2003</xref>), whilst responses associated with protective immunity, such as IgE, IgG1 and IgG3, tend to emerge later in infection in response antigens released from dying adult worms (Woolhouse and Hagan, <xref ref-type="bibr" rid="ref167">1999</xref>).</p><p>There are notable distinctions between the type and magnitude of the cytokine response to egg-specific antigens and those directed against adult worm antigens (Joseph <italic>et al.</italic> <xref ref-type="bibr" rid="ref79">2004</xref>; Silveira <italic>et al.</italic> <xref ref-type="bibr" rid="ref144">2004</xref>). Adult <italic>S. mansoni</italic> worms tend to elicit a mixed Th1-Th2 cytokine profile (Williams <italic>et al.</italic> <xref ref-type="bibr" rid="ref164">1994</xref>) and are less effective at stimulating <italic>in vitro</italic> granuloma formation (IVGF) than egg antigens (ElRidi <italic>et al.</italic> <xref ref-type="bibr" rid="ref40">1997</xref>). Cross-sectional data from an <italic>S. haematobium</italic> endemic cohort suggests that adult worm-specific effector Th2 cytokines increase whilst IL-10 titres decline with age/exposure to infection (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref116">2007</xref>) and thus effector responses to adult worms are higher in putatively resistant individuals.</p><p>In contrast to the Th2 cytokine responses induced by schistosome eggs and infective larvae of most nematodes, schistosome cercariae stimulate Th1/inflammatory mRNA expression in mice and resistance to larval invasion post-vaccination is dependent on IFN<italic>γ</italic> (Wynn <italic>et al.</italic> <xref ref-type="bibr" rid="ref168">1994</xref>). Although few studies have directly compared immune responses to the three schistosome life-cycle stages in humans, cercariae-specific IgM, IgG1 and IgG4 titres are higher than those directed against adult worm antigens (Viana <italic>et al.</italic> <xref ref-type="bibr" rid="ref159">1995</xref>). The distinct immune responses elicited by different helminth life-cycle stages underpin the development of so-called concomitant immunity, whereby <italic>de novo</italic> larval infection is blocked by adult worm-induced immunity but resident adult parasites are tolerated, a theory originally formulated for schistosome infections (Smithers and Terry, <xref ref-type="bibr" rid="ref146">1967</xref>). Studies have found evidence for development of PBMC-mediated resistance to L3 invasion in <italic>O. volvulus</italic> infection in an endemic area of Cameroon (MacDonald <italic>et al.</italic> <xref ref-type="bibr" rid="ref92">2002</xref>) and development of peripheral antibody-dependent immunity to <italic>W. bancrofti</italic> larvae with age in Papua New Guinea (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref27">1991<italic>a</italic></xref>,<xref ref-type="bibr" rid="ref28"><italic>b</italic></xref>). There is little evidence for development of concomitant immunity to GI nematode infections; however, there is a distinct paucity of data in this area.</p><p>In addition to influencing anti-parasite immunity, helminth life-cycle stage contributes to heterogeneity in anti-pathology immune responses. Immunomodulatory processes can be life cycle stage-specific as characterized by distinct cytokine and proliferative responses to their respective antigens (Geiger <italic>et al.</italic> <xref ref-type="bibr" rid="ref56">2007</xref>). <italic>In vitro</italic> microfilariae are able to impair cytokine expression and maturation of human dendritic cells (DCs) (Semnani <italic>et al.</italic> <xref ref-type="bibr" rid="ref142">2001</xref>, <xref ref-type="bibr" rid="ref141">2004</xref>) and schistosome egg antigens can inhibit co-stimulatory molecule expression and skew APC cytokine secretion from an inflammatory to regulatory profile (Correale and Farez, <xref ref-type="bibr" rid="ref23">2009</xref>), with potential implications for the systemic CD4+ T cell phenotype. A variety of studies have also shown that cercariae excretory/secretory products actively modulate the host immune response during migration and maturation independent of egg or adult-worm-mediated processes (reviewed by Jenkins <italic>et al.</italic> <xref ref-type="bibr" rid="ref77">2005</xref>). However, whilst eggs, cercariae and microfilariae can impair and polarize host responses, the ability of parasites to evade and modulate immune recognition seems to increase as they mature (Nutman and Kumaraswami, <xref ref-type="bibr" rid="ref120">2001</xref>) and corresponds to large-scale switches in many suites of genes (Jolly <italic>et al.</italic> <xref ref-type="bibr" rid="ref78">2007</xref>) and active secretion of immunomodulatory molecules (Geiger <italic>et al.</italic> <xref ref-type="bibr" rid="ref56">2007</xref>). Thus, despite being exposed to the host immune system for the longest of all life-cycle stages, it is unsurprising that adult worms are so resistant to immune-mediated clearance (Maizels and Yazdanbakhsh, <xref ref-type="bibr" rid="ref99">2003</xref>), while immature parasites tend to be immunogenic, more readily killed by effector immune responses (Viana <italic>et al.</italic> <xref ref-type="bibr" rid="ref159">1995</xref>; Semnani <italic>et al.</italic> <xref ref-type="bibr" rid="ref142">2001</xref>; Medeiros <italic>et al.</italic> <xref ref-type="bibr" rid="ref104">2003</xref>) and are responsible for the majority of morbidity in helminth infections (Maizels and Yazdanbakhsh, <xref ref-type="bibr" rid="ref99">2003</xref>).</p></sec><sec id="sec4-4"><title>Parasite life-span</title><p>Unlike microbial infections which multiply exponentially in their hosts, helminths have evolved to invest in immune-evasive mechanisms to prolong intra-host survival and long-term fecundity (Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref72">2009</xref>). Effective immune evasion and suppression by adult worms mean that reactivity to the antigens of live worms is limited (Geiger <italic>et al.</italic> <xref ref-type="bibr" rid="ref56">2007</xref>). Thus, hosts may only experience an immunogenic ‘threshold’ stimulus of parasite antigens once adult worms die (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref112">2008</xref>) and resistance might be predicted to develop more slowly against long-lived worms than against shorter-lived species. The rapid switch to a protective immune profile following anti-helminthic drug treatment that kills adult worms is consistent with this hypothesis (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref113">2003</xref>; Watanabe <italic>et al.</italic> <xref ref-type="bibr" rid="ref160">2007</xref>). If adult helminth life-span does cause a lag in the development of protective immunity then this may contribute to the variation in the age at which peak prevalence (Brooker <italic>et al.</italic> <xref ref-type="bibr" rid="ref15">2000</xref>) and infection intensity (<xref ref-type="fig" rid="fig02">Fig. 2</xref>) occurs in host populations exposed to different helminths.
<fig id="fig02" position="float"><label>Fig. 2</label><caption><p>The relationship between age and infection intensity in natural human helminthiases. (A) Mean <italic>W. bancrofti</italic> microfilaria (mf) count by age group (<italic>n</italic>=156, study area: Papua New Guinea, method: microscopy of 2 ml Giemsa-stained blood). Reprinted from the <italic>American Journal of Tropical Medicine and Hygiene</italic> (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref28">1991<italic>b</italic></xref>), with permission from the managing editor. (B) Mean hookworm (<italic>A. duodenale</italic> and <italic>N. americanus</italic>) egg counts per gram faeces (EPG) by age group (<italic>n</italic>=631, study area: China, method: Kato-Katz thick smear). Reprinted from the <italic>Journal of Parasitology</italic> (Gandhi <italic>et al.</italic> <xref ref-type="bibr" rid="ref55">2001</xref>), with permission from Allen Press Publishing Services. (C) Mean <italic>T. trichiuris</italic> eggs per gram of faeces by age group (<italic>n</italic>=96, study area: Cameroon, method: Kato-Katz thick smear). Reprinted from the <italic>Journal of Infectious Diseases</italic> (Faulkner <italic>et al.</italic> <xref ref-type="bibr" rid="ref45">2002</xref>), with permission from the University of Chicago Press. (D) Age-infection intensity profiles of <italic>S. haematobium</italic> egg counts per 10 ml of urine from an area of low infection prevalence (dashed line) and an area of high infection prevalence (solid line) group (<italic>n</italic>=133 and 147, study area: Zimbabwe, method: filtration of 10 ml of urine) (re-drawn from Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref115">1997</xref>). Reprinted from <italic>Parasitology Today</italic> (Woolhouse, <xref ref-type="bibr" rid="ref166">1998</xref>), with permission from Elsevier and John Wiley and Sons Ltd.</p></caption><graphic xlink:href="S0031182010001216_fig2"></graphic></fig></p><p>Additionally, whilst some helminths have been known to survive for extremely long periods (Vermund <italic>et al.</italic> <xref ref-type="bibr" rid="ref157">1983</xref>), most die before reaching their maximum longevity. It is possible that the relatively short average helminth life-span in immunocompetent individuals reaps the maximal reproductive success relative to the physiological cost to the parasite of evading and modulating the host immune response. In opposition to this, studies in hookworm suggest that the immune response has only a limited impact on parasite longevity (reviewed by Loukas and Prociv, <xref ref-type="bibr" rid="ref91">2001</xref>). Species with indirect life cycles, such as <italic>Schistosoma</italic> spp. and vector-borne helminths, tend to be long-lived (<xref ref-type="table" rid="tab01">Table 1</xref>). Thus, once adult worms have adapted to their optimal host niche, they can produce offspring over a long period and, whilst they are immunogenic, adult worms do not appear to be the primary targets of the anti-helminth immune response in humans or in animal models (Smithers and Terry, <xref ref-type="bibr" rid="ref146">1967</xref>). This may be particularly true of <italic>O. volvulus</italic>, which has an average adult life-span of 8–10 years, but can have a maturation delay in the human host of over a year (Anderson and May, <xref ref-type="bibr" rid="ref2">1985</xref>). For short-lived worms, such as <italic>E. vermicularis</italic>, maturation and oviposition occurs much earlier, with an associated shift in stage-specific immune responses (Anderson and May, <xref ref-type="bibr" rid="ref2">1985</xref>).</p></sec></sec><sec id="sec5"><title>GENETIC HETEROGENEITIES IN HELMINTH INFECTION</title><sec id="sec5-1"><title>Host genetics</title><p>The human immune system has evolved in the context of helminth infection and this relationship has led to significant changes in our immune genes (Fumagalli <italic>et al.</italic> <xref ref-type="bibr" rid="ref53">2009</xref>; Maizels, <xref ref-type="bibr" rid="ref94">2009</xref>). A recent comprehensive study of 91 interleukin genes in 52 human populations found evidence for balancing selection in the evolution of the human immune response driven by helminth ‘species richness’, i.e. the greater diversity of helminths to which a population has been exposed, the greater diversity observed in interleukin alleles (Fumagalli <italic>et al.</italic> <xref ref-type="bibr" rid="ref53">2009</xref>). These findings are consistent with helminths differentially affecting the human acquired immune response at all levels of the CD4+ T cell axis, including gene families involved in inflammation in the skin, mucosal immunity, cell proliferation and survival and Th2 cytokines (Fumagalli <italic>et al.</italic> <xref ref-type="bibr" rid="ref53">2009</xref>). This is compounded by earlier studies indicating that many of the key genetic loci controlling the balance of effector and regulatory responses are polymorphic in the human population (<xref ref-type="bibr" rid="ref129">Quinnell, 2003</xref>) and that certain human genes are associated with predisposition to infection with specific helminth parasites (Hoerauf <italic>et al.</italic> <xref ref-type="bibr" rid="ref68">2002</xref>; Peisong <italic>et al.</italic> <xref ref-type="bibr" rid="ref126">2004</xref>; Kouriba <italic>et al.</italic> <xref ref-type="bibr" rid="ref85">2005</xref>).</p><p>Additive genetic effects (heritability) significantly influence human infections with <italic>A. lumbricoides</italic> (Williams-Blangero <italic>et al.</italic> <xref ref-type="bibr" rid="ref163">2002<italic>b</italic></xref>), <italic>T. trichiura</italic> (Williams-Blangero <italic>et al.</italic> <xref ref-type="bibr" rid="ref162">2002<italic>a</italic></xref>), and <italic>S. mansoni</italic> (Bethony <italic>et al.</italic> <xref ref-type="bibr" rid="ref7">2002</xref>), whilst other studies have found host genetics to be less influential relative to exposure history (King <italic>et al.</italic> <xref ref-type="bibr" rid="ref82">2004</xref>). This conflicting evidence suggests that helminth distribution, allele frequency and host behaviour in each locality may determine the relative importance of heritable factors in patterns of infection and immunity (Ellis <italic>et al.</italic> <xref ref-type="bibr" rid="ref38">2007</xref>). Familial clustering of infection can further confound identification of genetic factors associated with helminth infection since <italic>in utero</italic> sensitization via transfer of helminth antigens and soluble immune factors from infected mothers to their offspring is independent of genotype (Eloi-Santos <italic>et al.</italic> <xref ref-type="bibr" rid="ref39">1989</xref>; Lammie <italic>et al.</italic> <xref ref-type="bibr" rid="ref87">1991</xref>; Novato-Silva <italic>et al.</italic> <xref ref-type="bibr" rid="ref119">1992</xref>) and co-habiting families often have similar exposure patterns (Smith <italic>et al.</italic> <xref ref-type="bibr" rid="ref145">2001</xref>). <italic>T. trichiura</italic> and <italic>A. lumbricoides</italic> for example were found to be significantly associated with shared living conditions; however, when infection distribution was investigated in more depth, only <italic>T. trichiura</italic> infection intensity was heritable (Ellis <italic>et al.</italic> <xref ref-type="bibr" rid="ref38">2007</xref>). In addition, populations in historically stable endemic areas may exhibit less heritable variation in host susceptibility if long-term selection against genotypes less favourable for a specific infection has occurred (King <italic>et al.</italic> <xref ref-type="bibr" rid="ref82">2004</xref>), particularly where other species of helminth infection are uncommon (Fumagalli <italic>et al.</italic> <xref ref-type="bibr" rid="ref53">2009</xref>).</p><p>Multiple gene loci have now been implicated in determining the degree of resistance to helminthiases and while many appear to relate to individual helminth species (reviewed by Quinnell, <xref ref-type="bibr" rid="ref129">2003</xref>), there are also loci controlling multiple susceptibilities, as is the case for IL-13 polymorphisms associated with predisposition to <italic>S. haematobium</italic> (Kouriba <italic>et al.</italic> <xref ref-type="bibr" rid="ref85">2005</xref>) and <italic>O. volvulus</italic> (Hoerauf <italic>et al.</italic> <xref ref-type="bibr" rid="ref68">2002</xref>).</p></sec><sec id="sec5-2"><title>Parasite genetics</title><p>Widespread genetic variation between parasite species is an equally important source of heterogeneity in the development of acquired immune responses to infection. Since parasitic nematodes have arisen from several independent evolutionary pathways their classification within the Phylum <italic>Nematoda</italic> belies the huge diversity apparent from their distinct life-histories, physiology and proteomes (Dorris <italic>et al.</italic> <xref ref-type="bibr" rid="ref37">1999</xref>). Comparisons between nematode worms at the genomic level have identified multiple species-specific gene sequences and transcription patterns, even between phylogenetically close organisms (Parkinson <italic>et al.</italic> <xref ref-type="bibr" rid="ref123">2004</xref>). Among the 3 major human <italic>Schistosoma</italic> spp. differences in immunologically relevant antigens have been found. Notably the leading anti-schistosome vaccine candidate antigen; glutathione-S-transferase (GST), of <italic>S. mansoni</italic> differs from that of <italic>S. haematobium</italic> (Trottein <italic>et al.</italic> <xref ref-type="bibr" rid="ref152">1992</xref>), though the impact of this on human immunity is unknown.</p><p>The existence of helminth homologues of human proteins (Pastrana <italic>et al.</italic> <xref ref-type="bibr" rid="ref124">1998</xref>; Gomez-Escobar <italic>et al.</italic> <xref ref-type="bibr" rid="ref59">2000</xref>) and analyses that indicate more rapid evolution among parasite secreted proteins are compatible with the idea that parasitic helminths are diversifying fastest among antigens exposed to (and interacting with) the host immune system (Hoekstra <italic>et al.</italic> <xref ref-type="bibr" rid="ref67">2000</xref>; Harcus <italic>et al.</italic> <xref ref-type="bibr" rid="ref62">2004</xref>). The relatively recent completion of the first parasitic nematode (<italic>B. malayi</italic>; Ghedin <italic>et al.</italic> <xref ref-type="bibr" rid="ref58">2007</xref>) and trematode genome projects (<italic>S. mansoni</italic>; Berriman <italic>et al.</italic> <xref ref-type="bibr" rid="ref6">2009</xref>) and <italic>S. japonicum</italic> (Zhou <italic>et al.</italic> <xref ref-type="bibr" rid="ref171">2009</xref>) will inevitably yield greater insights into the evolution of genetic diversity between different helminth species.</p><p>Genetic diversity within helminth species may partly explain the slow development of protective immunity in endemic populations. It has been proposed that natural infections consist of several genetically distinct parasite strains (Galvani, <xref ref-type="bibr" rid="ref54">2005</xref>), evidence for which comes from variations in the non-coding sequence identified via genome-wide scans (Hunt <italic>et al.</italic> <xref ref-type="bibr" rid="ref71">2008</xref>; Redman <italic>et al.</italic> <xref ref-type="bibr" rid="ref133">2008</xref>). The effect of helminth strains on the host immune response has been investigated in theoretical models based on field studies of <italic>A. lumbricoides, N. americanus, S. haematobium</italic> and <italic>T. trichiura</italic> infections, which surmise that challenge with multiple strains delays development of resistance to infection in human populations because a different protective response must be mounted against each parasite genotype separately (Galvani, <xref ref-type="bibr" rid="ref54">2005</xref>).</p></sec></sec><sec id="sec6"><title>INDIVIDUAL EXPOSURE HISTORY</title><p>The immune environment to which <italic>de novo</italic> helminth infections are exposed is not independent of a host's infection history (Woolhouse and Hagan, <xref ref-type="bibr" rid="ref167">1999</xref>). This was first demonstrated in a study of Sudanese canal workers hyper-exposed to <italic>S. mansoni</italic> infection, which showed that those who had been occupationally exposed for over 10 years were more resistant to infection than newly recruited workers (Satti <italic>et al.</italic> <xref ref-type="bibr" rid="ref136">1996</xref>). More recently a direct comparison between 2 occupationally exposed male cohorts, found that chronically exposed individuals develop resistance to <italic>S. mansoni</italic> re-infection after significantly fewer rounds of praziquantel treatment than those with a shorter exposure history (Black <italic>et al.</italic> <xref ref-type="bibr" rid="ref8">2010</xref>).</p><p>It is well known that in endemic populations worm burdens accumulate with age to a peak intensity and decline thereafter (Fisher, <xref ref-type="bibr" rid="ref48">1934</xref>) but the age at which peak prevalence occurs (Brooker <italic>et al.</italic> <xref ref-type="bibr" rid="ref15">2000</xref>) and the relative decline post-peak varies according to helminth species (<xref ref-type="fig" rid="fig02">Fig. 2</xref>). For example, intensity of <italic>W. bancrofti</italic> (<xref ref-type="fig" rid="fig02">Fig. 2</xref>A) and hookworm (<xref ref-type="fig" rid="fig02">Fig. 2</xref>B) infections tends to be highest in adults rather than children (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref28">1991<italic>b</italic></xref>; Gandhi <italic>et al.</italic> <xref ref-type="bibr" rid="ref55">2001</xref>). In contrast, <italic>T. trichiuria</italic> (<xref ref-type="fig" rid="fig02">Fig. 2</xref>C) and schistosome (<xref ref-type="fig" rid="fig02">Fig. 2</xref>D) infection intensity peaks in childhood, after which worm burdens decline (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref115">1997</xref>; Faulkner <italic>et al.</italic> <xref ref-type="bibr" rid="ref45">2002</xref>). Host behaviour may partially explain these differences, for example the risk of hookworm infection is highest in adults due to occupation-related exposure (Bradley and Chandiwana, <xref ref-type="bibr" rid="ref11">1990</xref>), whilst exposure to schistosomiasis is determined by contact with water from an early age during washing and domestic activities (Rudge <italic>et al.</italic> <xref ref-type="bibr" rid="ref134">2008</xref>).</p><p>Evidence that the host immune response is important in shaping age-related variation includes the observation that peak worm burdens occur at a younger age in regions of high infection intensity than in regions with low or intermediate intensity, a phenomenon called the ‘peak shift’ (Woolhouse, <xref ref-type="bibr" rid="ref166">1998</xref>) (<xref ref-type="fig" rid="fig02">Fig. 2</xref>D). It is clear that, at least for long-term residents of an area endemic for a particular species of helminth, age is effectively a proxy of exposure history and cumulative exposure to parasite antigens over time can trigger changes in the immune response (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref112">2008</xref>). The latter assertion is supported by immuno-epidemiological studies in a variety of helminthiases indicating that cellular and humoral changes correlate with development of resistance to infection with age. For example in an <italic>S. haematobium</italic>-infected population, cross-sectional data showed that cytokine responses switch from a regulatory IL-10 response in younger individuals to an effector IL-5 response in older individuals (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref116">2007</xref>). Longitudinal studies of <italic>W. bancrofti-</italic>infected subjects in Papua New Guinea showed that adults are relatively resistant to parasite accrual (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref28">1991<italic>b</italic></xref>) and that this could be attributed to parallel age-specific acquisition of anti-larval antibodies (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref27">1991<italic>a</italic></xref>). As discussed above, development of this form of concomitant immunity may be one explanation for the lower prevalence of these species in adults (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref27">1991<italic>a</italic></xref>,<xref ref-type="bibr" rid="ref28"><italic>b</italic></xref>; MacDonald <italic>et al.</italic> <xref ref-type="bibr" rid="ref92">2002</xref>).</p><p>In areas of high intensity transmission, people are exposed to infection from a very early age and these patterns vary according to parasite species (Sousa-Figueiredo <italic>et al.</italic> <xref ref-type="bibr" rid="ref147">2008</xref>). A recent study in Zanzibar found that whilst schistosome infections were rare in pre-school children, soil-transmitted helminths were already highly prevalent (Sousa-Figueiredo <italic>et al.</italic> <xref ref-type="bibr" rid="ref147">2008</xref>). Variation in maternal infection status may also introduce variation in the <italic>in utero</italic> exposure patterns and potentially lead to long-lasting effects on the anti-helminth immune response of their offspring. For example, Steel and colleagues showed that pre-natal priming during maternal helminth infection has far-reaching effects on anti-filarial immunity including clonal deletion of parasite-specific T cells (Steel <italic>et al.</italic> <xref ref-type="bibr" rid="ref148">1994</xref>) and life-long susceptibility to infection (Steel and Nutman, <xref ref-type="bibr" rid="ref149">2003</xref>). Cellular studies in endemic populations have shown that umbilical cord blood lymphocytes (CBL) from neonates born of <italic>W. bancrofti</italic>-infected mothers mount parasite-specific cytokine responses similar to those of maternal PBMCs and in contrast to neonates born of un-infected mothers (Malhotra <italic>et al.</italic> <xref ref-type="bibr" rid="ref101">1997</xref>). An extension of this study found that schistosome and <italic>B. malayi</italic>-specific cytokine responses persisted in childhood and significantly affected the CD4+ T cell polarization of <italic>Bacillus</italic> Calmette-Guerin (BCG) vaccine-specific responses in 2 to 10 year olds (Malhotra <italic>et al.</italic> <xref ref-type="bibr" rid="ref100">1999</xref>). However, an investigation of CBL responses to <italic>N. americanus</italic> and <italic>O. volvulus</italic> antigens found no evidence for specific polarization of Th1 and Th2 responses in the offspring of helminth-infected mothers (Pit <italic>et al.</italic> <xref ref-type="bibr" rid="ref127">2000</xref>). To date only a very few studies have directly compared the effect of different helminth species on neonatal immunity, though researchers hypothesize that tissue-dwelling helminths may be associated with a greater trans-placental transfer of antigens (Eloi-Santos <italic>et al.</italic> <xref ref-type="bibr" rid="ref39">1989</xref>; Novato-Silva <italic>et al.</italic> <xref ref-type="bibr" rid="ref119">1992</xref>; Malhotra <italic>et al.</italic> <xref ref-type="bibr" rid="ref101">1997</xref>). Since maternal exposure patterns will inevitably affect neonatal and early post-natal exposure the contribution of parasite transmission route and the associated behavioural risk factors for infection to immune heterogeneity (discussed above) should not be overlooked in early life.</p></sec><sec id="sec7"><title>ANTI-HELMINTHIC TREATMENT</title><p>Anti-helminthic treatment can effectively clear infection and thus artificially disrupts host-parasite immunoepidemiology, for example immune reactivity has been shown to peak shortly after treatment in many species of helminth infection (Quinnell <italic>et al.</italic> <xref ref-type="bibr" rid="ref130">2004</xref>; Watanabe <italic>et al.</italic> <xref ref-type="bibr" rid="ref160">2007</xref>). Following treatment, however, endemic populations become re-infected and the highest re-infection rates are consistently seen in individuals who carried high worm burdens before treatment suggesting pre-disposition to infection in certain hosts (Bundy <italic>et al.</italic> <xref ref-type="bibr" rid="ref16">1988</xref>; Tingley <italic>et al.</italic> <xref ref-type="bibr" rid="ref151">1988</xref>; Chandiwana <italic>et al.</italic> <xref ref-type="bibr" rid="ref19">1991</xref>).</p><p>In addition to clearing infection, even a single dose of chemotherapy can lead to changes in the host immune response to helminths. Successful treatment has been shown to enhance the proportion of effector T cells (Watanabe <italic>et al.</italic> <xref ref-type="bibr" rid="ref160">2007</xref>), increase the range of parasite proteins recognized by host antibodies and induce a more rapid switch to protective antibody isotypes (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref113">2003</xref>) in schistosomiasis patients. This post-treatment rebound in immune responsiveness could be due to heightened DC activation in an environment of high parasite death (Watanabe <italic>et al.</italic> <xref ref-type="bibr" rid="ref160">2007</xref>) and/or recovery of normal immune function following removal of immunosuppressive parasite excretory/secretory products (Maizels and Yazdanbakhsh, <xref ref-type="bibr" rid="ref99">2003</xref>).</p><p>Furthermore, the large variation in treatment regimens employed in mass-treatment programmes, including the drug administered, number of treatments (single or repeated dose), age-ranges targeted (e.g. school-age children, whole population) and method of administration (e.g. school-based, hospital/clinic-based), is also a potential source of variation in host immunity within endemic populations. Notably, many treatment programmes exclude children under the age of 5 due to a perceived risk of side-effects, despite evidence that children can become both infected and a source of transmission from a very young age (Opara <italic>et al.</italic> <xref ref-type="bibr" rid="ref121">2007</xref>). Most also employ single-dose regimens, despite evidence that repeated treatment may be more effective at augmenting protective immunity (Black <italic>et al.</italic> <xref ref-type="bibr" rid="ref8">2010</xref>) potentially by periodically ‘boosting’ development of immunological memory (Woolhouse and Hagan, <xref ref-type="bibr" rid="ref167">1999</xref>). Whilst the long-term effects of anti-helminthic treatment on the host acquired immune response remain unclear, the desired reduction in parasite prevalence and transmission inevitably impacts upon helminth immunoepidemiology.</p></sec><sec id="sec8"><title>CO-INFECTION</title><p>Co-infection adds a further level of complexity to host-pathogen interactions and is highly prevalent in some communities, particularly in sub-Saharan Africa (Raso <italic>et al.</italic> <xref ref-type="bibr" rid="ref131">2004</xref>; Brooker <italic>et al.</italic> <xref ref-type="bibr" rid="ref14">2006</xref>). Here we focus on how co-infections of particular public health significance contribute to heterogeneity in the anti-helminth immune response and how these effects vary depending on the species of helminth infection.</p><sec id="sec8-1"><title>Helminth-helminth co-infection</title><p>Certain combinations of helminth co-infection are more common in human populations than others, notably several nematode pairs including: <italic>A. lumbricoides</italic> and <italic>T. trichiura</italic> (Faulkner <italic>et al.</italic> <xref ref-type="bibr" rid="ref44">2005</xref>; Ellis <italic>et al.</italic> <xref ref-type="bibr" rid="ref38">2007</xref>), <italic>A. lumbricoides</italic> and hookworm (Fleming <italic>et al.</italic> <xref ref-type="bibr" rid="ref50">2006</xref>) and <italic>O. volvulus</italic> and <italic>T. trichiura</italic> (Faulkner <italic>et al.</italic> <xref ref-type="bibr" rid="ref44">2005</xref>). Interactions between schistosomes and nematodes in co-infection are more variable, with evidence for co-aggregation with hookworms (Fleming <italic>et al.</italic> <xref ref-type="bibr" rid="ref50">2006</xref>) and <italic>T. trichiura</italic> (Ellis <italic>et al.</italic> <xref ref-type="bibr" rid="ref38">2007</xref>), but no significant association with <italic>A. lumbricoides</italic> infection intensity (Tchuem Tchuente <italic>et al.</italic> <xref ref-type="bibr" rid="ref150">2003</xref>; Fleming <italic>et al.</italic> <xref ref-type="bibr" rid="ref50">2006</xref>; Ellis <italic>et al.</italic> <xref ref-type="bibr" rid="ref38">2007</xref>). Co-infection also tends to be associated with higher worm burdens than those seen in single species infections (Tchuem Tchuente <italic>et al.</italic> <xref ref-type="bibr" rid="ref150">2003</xref>). <italic>A. lumbricoides-T. trichiura</italic> co-infected individuals were also found to have higher IgG4:IgE ratios than their singly-infected counterparts (Figueiredo <italic>et al.</italic> <xref ref-type="bibr" rid="ref46">2010</xref>).</p><p>Several explanations for the variable effect of one helminth species on the likelihood of co-infection with another have been proposed, although it is unlikely that these factors act in isolation. Firstly, similarities in parasite life cycle might mean that certain species share common behavioural or genetic risk factors for infection (Ellis <italic>et al.</italic> <xref ref-type="bibr" rid="ref38">2007</xref>; Pullan <italic>et al.</italic> <xref ref-type="bibr" rid="ref128">2008</xref>). Alternatively, since studies in animals and humans show that patent infection with one helminth species can depress both the humoral and cellular responses of the host to challenge by other parasites (Brady <italic>et al.</italic> <xref ref-type="bibr" rid="ref12">1999</xref>; Correa-Oliveira <italic>et al.</italic> <xref ref-type="bibr" rid="ref22">2002</xref>) it is possible that these synergistic interactions result from non-specific ‘bystander suppression’ (Brady <italic>et al.</italic> <xref ref-type="bibr" rid="ref12">1999</xref>) or immunosuppression directed against cross-reactive antigens expressed by closely-related species (Geiger <italic>et al.</italic> <xref ref-type="bibr" rid="ref57">2002</xref>). <italic>S. mansoni</italic>-exposed but patently uninfected Brazilian subjects, identified by egg and adult worm-specific antibodies, were found to have impaired responses to <italic>Ascaris</italic> spp. and hookworm infections (Correa-Oliveira <italic>et al.</italic> <xref ref-type="bibr" rid="ref22">2002</xref>), suggesting that prior exposure to schistosomiasis may have a lasting impact on host responses to other helminths. Experimental studies comparing <italic>S. mansoni</italic> infection with antigen (adult worm and egg homogenates) administration, suggest that immunosuppressive mechanisms rely on the presence of active infection (Osada and Kanazawa, <xref ref-type="bibr" rid="ref122">2010</xref>). However there is a lack of data on the effect of exposure to one parasite on the immunobiology of subsequent infection with a different species. It is conceivable that, even after clearance of adult worms, sequestration of eggs in host tissues, cellular memory responses to cross-reactive antigens and impaired organ-function resulting from cumulative morbidity may all affect the response to subsequent helminthiases.</p></sec><sec id="sec8-2"><title>Helminth-malaria co-infection</title><p>Malaria is a predominantly intracellular protozoan infection and has a markedly different immunobiology to that of helminths. The host response to malaria is characterized by inflammatory cytokines causing periodic fevers and immune-mediated pathology and, though protective immunity is yet to be fully characterized, clearance of blood-stage infection positively correlates with titres of variant-specific cytophilic antibodies, particularly IgG3 (Cavanagh <italic>et al.</italic> <xref ref-type="bibr" rid="ref18">2004</xref>).</p><p>Studies of the effect of malaria on immune responses to helminths are rare and tend to focus on the anti-malarial, rather than anti-helminth immune response. However, work on schistosomiasis-malaria co-infections indicate distinct effects on humoral and cellular responses (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref114">2000</xref>; Wilson <italic>et al.</italic> <xref ref-type="bibr" rid="ref165">2008</xref>). On the one hand, co-infection has been associated with elevated titres of schistosome egg-specific IgE and IgG3 (Mutapi <italic>et al.</italic> <xref ref-type="bibr" rid="ref114">2000</xref>), indicating that acute inflammatory responses to malaria may reverse helminth-mediated immune hyporesponsiveness. Consistent with this hypothesis, skewing of T cell responses by malaria can exacerbate liver and spleen pathology due to deficient regulation of schistosome egg-specific regulatory responses (Wilson <italic>et al.</italic> <xref ref-type="bibr" rid="ref165">2008</xref>). Recent schistosome-malaria co-infection studies also show that co-infected children do not differ from singly infected children in their absolute numbers of circulating Tregs, but do exhibit reduced proportions of memory Tregs (Muok <italic>et al.</italic> <xref ref-type="bibr" rid="ref110">2009</xref>). Both elevated malaria-specific IgG3 and high <italic>S. mansoni</italic> egg counts are risk factors for splenomegaly (Booth <italic>et al.</italic> <xref ref-type="bibr" rid="ref10">2004<italic>b</italic></xref>), suggesting that both severity of infection and host immunoreactivity contribute to the clinical outcome of malaria-schistosome co-infection (Diallo <italic>et al.</italic> <xref ref-type="bibr" rid="ref34">2004</xref>).</p><p>In individuals concurrently infected with GI nematodes and malaria, the inflammatory response to <italic>Plasmodium</italic> spp. might be expected to blunt Th2 effector responses involved in clearance of adult nematodes (Mountford and Pearlman, <xref ref-type="bibr" rid="ref109">1998</xref>). For example, <italic>N. americanus</italic>-specific Th2 effector cytokine and total IgE responses were lower in Papua New Guinean subjects co-infected with malaria, despite no observable effect on hookworm-specific IFN<italic>γ</italic> or cell proliferation (Quinnell <italic>et al.</italic> <xref ref-type="bibr" rid="ref130">2004</xref>). The same study found evidence for malaria and hookworm-mediated suppression of cell proliferation, but not effector cytokine secretion, in response to bacterial antigens (Quinnell <italic>et al.</italic> <xref ref-type="bibr" rid="ref130">2004</xref>). Thus, malaria co-infection can limit the effector response to hookworm, but may not significantly affect hookworm-mediated immunosuppressive mechanisms. Conversely, in a Malian study of malaria-<italic>W. bancrofti</italic> co-infection, filariasis was significantly associated with elevated total and malaria-specific IL-10 and reduced IFN<italic>γ</italic> (Metenou <italic>et al.</italic> <xref ref-type="bibr" rid="ref106">2009</xref>). As more co-infection studies are conducted it will become possible to more directly compare effects of malaria on the acquired immune responses mounted against different helminth species.</p></sec><sec id="sec8-3"><title>Helminth-HIV co-infection</title><p>Human Immunodeficiency Virus (HIV) is a lymphotrophic virus that replicates in CD4+ T cells leading to incremental abrogation of this cell population and progression to Acquired Immune Deficiency Syndrome (AIDS). Both HIV and helminth infection can be considered as immunocompromising infections, and it could therefore be predicted that these effects would synergise to the detriment of co-infected hosts.</p><p>Although co-infection studies tend to focus on immune responses to HIV, there is some evidence for heterogeneity in the reciprocal effects of HIV on helminth immunobiology. For example, HIV infection is associated with up-regulation of CTLA-4 expression and anergy, which might enhance helminth-mediated Treg induction and immune evasion (Steel and Nutman, <xref ref-type="bibr" rid="ref149">2003</xref>; Leng <italic>et al.</italic> <xref ref-type="bibr" rid="ref89">2006</xref>). Severe immunosuppression in advanced HIV/AIDS is also linked to abnormally high intensity <italic>Strongyloides</italic> spp. infections due to increased rates of auto-infection and, in some regions, strongyloidiasis is considered to be an AIDS-related opportunistic infection (Meamar <italic>et al.</italic> <xref ref-type="bibr" rid="ref103">2007</xref>). Furthermore, low CD4+ T cell counts in HIV seropositive individuals has been associated with increased tissue sequestration of schistosome eggs (Karanja <italic>et al.</italic> <xref ref-type="bibr" rid="ref81">1997</xref>), although the relative impact that this has on host pathology has not been investigated.</p><p>In addition to generalized immunosuppression, HIV co-infections are negatively correlated with worm-specific effector cytokine responses (Sentongo <italic>et al.</italic> <xref ref-type="bibr" rid="ref143">1998</xref>) and may therefore reduce clearance of both adult and immature worms. HIV-positive patients co-infected with <italic>S. mansoni</italic> had lower measurable agonist-specific IL-4 and parasite and agonist-specific IL-10 than their HIV-negative counterparts, but had similar levels of IFN<italic>γ</italic> (Mwinzi <italic>et al.</italic> <xref ref-type="bibr" rid="ref117">2001</xref>). This finding was linked to an increased Th1:Th2 effector cytokine ratio in HIV-positive individuals (Mwinzi <italic>et al.</italic> <xref ref-type="bibr" rid="ref117">2001</xref>), which may result from preferential infection and abrogation of activated Th2 cells relative to Th1 and naïve T cells (Maggi <italic>et al.</italic> <xref ref-type="bibr" rid="ref93">1994</xref>).</p><p>Disruption of CD4+ T cell polarization and regulatory mechanisms might be predicted to exacerbate helminth-related pathologies (Maggi <italic>et al.</italic> <xref ref-type="bibr" rid="ref93">1994</xref>; Booth <italic>et al.</italic> <xref ref-type="bibr" rid="ref9">2004<italic>a</italic></xref>), particularly in GI infections which require robust Th2 cytokine responses for clearance. However, very few studies of nematode-HIV co-infected populations have been conducted to date. HIV co-infection with schistosomiasis did not affect anti-helminthic treatment efficacy in a Kenyan cohort with high intensity <italic>S. mansoni</italic> infections (Karanja <italic>et al.</italic> <xref ref-type="bibr" rid="ref80">1998</xref>). Researchers in the latter study hypothesized that these findings were partly due to schistosomiasis preceding HIV infection and that subsequent co-infection did not affect pre-existing immune responses to schistosome antigens (Secor <italic>et al.</italic> <xref ref-type="bibr" rid="ref140">2004</xref>). The latter is of particular interest given that HIV is most prevalent in sexually-active adults and thus co-infections tend to arise after initial exposure to helminth infections, which peak in intensity in childhood. Thus, the stage of HIV infection (and associated degree of immunosuppression) and population-specific age-infection intensity distributions of different helminthiases are potential sources of heterogeneity and should be considered when investigating the immunobiology of co-infections.</p></sec></sec><sec sec-type="conclusion" id="sec9"><title>CONCLUSIONS</title><p>Parasitic helminths present a diverse challenge to the immune system. Their large proteome and broad-range of antigens alone may partially explain the slow development of resistance to helminthiases (Yazdanbakhsh and Sacks, <xref ref-type="bibr" rid="ref169">2010</xref>). Furthermore, the stage-specific challenges (Day <italic>et al.</italic> <xref ref-type="bibr" rid="ref27">1991<italic>a</italic></xref>,<xref ref-type="bibr" rid="ref28"><italic>b</italic></xref>; MacDonald <italic>et al.</italic> <xref ref-type="bibr" rid="ref92">2002</xref>) and genetic diversity within single species infections (Galvani, <xref ref-type="bibr" rid="ref54">2005</xref>) can lead to heterogeneity in anti-helminth immune responses in an individual host.</p><p>When comparing different species of helminth it is clear that immune-heterogeneity can transcend phylogenetic delineations, particularly with respect to parasite life-span and intra-host niche. Long-lived parasites and species inhabiting host tissues can only exist incognito via sophisticated immunosuppressive mechanisms that may compromise fecundity and transmission of infection (Karanja <italic>et al.</italic> <xref ref-type="bibr" rid="ref81">1997</xref>; Maizels and Yazdanbakhsh, <xref ref-type="bibr" rid="ref99">2003</xref>; Brattig, <xref ref-type="bibr" rid="ref13">2004</xref>). Short-lived and GI parasites face different challenges resulting in characteristic immunobiology. Whilst immunity to the tissue-dwelling nematodes is associated with a mixed CD4+ T cell immune response (Turaga <italic>et al.</italic> <xref ref-type="bibr" rid="ref154">2000</xref>), expulsion of GI nematode species is more specifically Th2-dependent (Turner <italic>et al.</italic> <xref ref-type="bibr" rid="ref155">2003</xref>). Few studies have directly compared immune responses to GI nematodes, filarial nematodes and <italic>Schistosoma</italic> spp. in single-infections, potentially due to the high prevalence of co-infection, meaning that many of the hypothesized sources of inter-specific immune heterogeneities remain to be empirically tested.</p><p>Unlike in experimental animal infections, acquired immune heterogeneity in natural infections also arises from host variables. Genetic polymorphism in the human immune system inevitably translates into heterogeneous expression of cellular and humoral responses, as is evident in clustering of immune responses within populations and individual families (Quinnell, <xref ref-type="bibr" rid="ref129">2003</xref>; Ellis <italic>et al.</italic> <xref ref-type="bibr" rid="ref38">2007</xref>). The relatively recent discovery of new CD4+ T cell subclasses and identification of further plasticity in innate effector cells has led to re-evaluation of how helminths interact with their human host (Diaz and Allen, <xref ref-type="bibr" rid="ref35">2007</xref>; Jenkins and Allen, <xref ref-type="bibr" rid="ref76">2010</xref>). Furthermore, the influence that host exposure-history, anti-helminthic treatment and co-infection have on anti-helminth responses indicates that immune heterogeneity arises not from the host and parasite in isolation, but also from the environment in which they interact.</p><p>Despite the diversity of helminth species and their host populations identifying the immunological mechanisms underlying these distinctions has been a challenge for field studies. Helminth-specific immune responses become activated and polarized at a very young age (Eloi-Santos <italic>et al.</italic> <xref ref-type="bibr" rid="ref39">1989</xref>; Lammie <italic>et al.</italic> <xref ref-type="bibr" rid="ref87">1991</xref>; Novato-Silva <italic>et al.</italic> <xref ref-type="bibr" rid="ref119">1992</xref>; Steel <italic>et al.</italic> <xref ref-type="bibr" rid="ref148">1994</xref>; King <italic>et al.</italic> <xref ref-type="bibr" rid="ref83">1998</xref>). However, field studies often exclude individuals under the age of 5, focusing instead on older individuals in the chronic stage of infection with a more ambiguous exposure and treatment history. In addition, whilst co-evolution of humans and helminths has clearly led to shared features of an anti-macroparasite response (Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref72">2009</xref>), it is also possible that peripheral sampling methods, co-infection and long-term systemic disease may disguise integral differences in human immune responses (Hayes <italic>et al.</italic> <xref ref-type="bibr" rid="ref63">2004</xref>). The cellular targets of systemic and highly pleiotropic cytokines and site-specific immune responses are particularly difficult to define in peripheral blood samples. Thus, in addition to expansion of elegant <italic>in vitro</italic> cellular assays, a wider range of immune correlates should be measured in the field to give a broader characterization of the host immune ‘phenotype’ in which these cells act.</p><p>Anthropophilic helminths are both evolutionarily ancient and alarmingly prevalent (Hotez <italic>et al.</italic> <xref ref-type="bibr" rid="ref70">2008</xref>), yet the immune responses mounted against them and the best means of treating infection remain unclear. Characterization of risk factors for infection and morbidity requires immunological measures to be considered in the context of host and environmental variables, which can be as influential as those of the parasite, and in some cases more so (Jackson <italic>et al.</italic> <xref ref-type="bibr" rid="ref73">2004<italic>a</italic></xref>; Ellis <italic>et al.</italic> <xref ref-type="bibr" rid="ref38">2007</xref>).</p></sec></body><back><ack><title>ACKNOWLEDGEMENTS</title><p>The authors would like to thank the <italic>American Journal of Tropical Medicine and Hygiene</italic>, Allen Press Publishing Services, the University of Chicago Press, Elsevier and John Wiley and Sons Ltd for permission to re-print published material. Financial support was provided by the Biotechnology and Biological Sciences Research Council, The Cunningham Trust, The Carnegie Trust for the Universities of Scotland, University of Edinburgh's Moray Endowment Fund, Tenovus Scotland and The Wellcome Trust (Grant numbers WT082028MA, 076561 and 090281). The Wellcome Trust also provided funding for this article to be made available in an Open Access environment.</p></ack><ref-list><title>REFERENCES</title><ref id="ref1"><mixed-citation publication-type="journal"><name><surname>Acosta</surname><given-names>L. P.</given-names></name><name><surname>McManus</surname><given-names>D. P.</given-names></name><name><surname>Aligui</surname><given-names>G. D. L.</given-names></name><name><surname>Olveda</surname><given-names>R. M.</given-names></name><name><surname>Tiu</surname><given-names>W. 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