Modulation of Specific and Allergy‐Related Immune Responses by Helminths

Daniłowicz-Luebert, Emilia; O’Regan, Noëlle Louise; Steinfelder, Svenja; Hartmann, Susanne

doi:10.1155/2011/821578

Cited by 52 publications

(59 citation statements)

References 181 publications

(196 reference statements)

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“…Suppressed lymphocyte responses were described in the 1970s (9), but the evidence base has not moved much beyond animal models and cross-sectional studies in humans (10). The cellular mechanisms associated with helminth-related immune hyporesponsiveness are not fully understood.…”

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confidence: 99%

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Community deworming alleviates geohelminth-induced immune hyporesponsiveness

Wammes

Hamid

Wiria

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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In cross-sectional studies, chronic helminth infections have been associated with immunological hyporesponsiveness that can affect responses to unrelated antigens. To study the immunological effects of deworming, we conducted a cluster-randomized, double-blind, placebo-controlled trial in Indonesia and assigned 954 households to receive albendazole or placebo once every 3 mo for 2 y. Helminthspecific and nonspecific whole-blood cytokine responses were assessed in 1,059 subjects of all ages, whereas phenotyping of regulatory molecules was undertaken in 121 school-aged children. All measurements were performed before and at 9 and 21 mo after initiation of treatment. Anthelmintic treatment resulted in significant increases in proinflammatory cytokine responses to Plasmodium falciparum-infected red blood cells (PfRBCs) and mitogen, with the largest effect on TNF responses to PfRBCs at 9 moestimate [95% confidence interval], 0.37 [0.21-0.53], P value over time (P time ) < 0.0001. Although the frequency of regulatory T cells did not change after treatment, there was a significant decline in the expression of the inhibitory molecule cytotoxic T lymphocyteassociated antigen 4 (CTLA-4) on CD4 + T cells of albendazoletreated individuals, -0.060 [-0.107 to -0.013] and -0.057 [-0.105 to -0.008] at 9 and 21 mo, respectively; P time = 0.017. This trial shows the capacity of helminths to up-regulate inhibitory molecules and to suppress proinflammatory immune responses in humans. This could help to explain the inferior immunological responses to vaccines and lower prevalence of inflammatory diseases in low-compared with high-income countries.helminths | albendazole | cytokine responses | Indonesia | deworming S oil-transmitted helminths (STHs) represent the most common infectious disease worldwide (1). In addition to specific worm-associated morbidities, it has been argued that chronic STH infections may magnify health-related burdens in communities remote from health care facilities, exacerbating anemia, poor nutritional status, and possibly poor cognitive development (1). However, this was not fully supported by the latest analysis of the Cochrane database (2).Immunologically, cellular immune hyporesponsiveness is a hallmark of chronic helminth infections that may allow parasites' longterm survival (3). The consequences of immunosuppression are manifold with potentially major public health relevance. Immune hyporesponsiveness could curtail effective immune responses, thereby increasing susceptibility to pathogens, and helminths are associated with suboptimal vaccine responses (4-6). The helminthrelated dampened immune responses might nevertheless help to prevent immunopathology during coinfections and, possibly, aberrant reactivity to environmental or self-antigens (7). With respect to the latter, there is currently much interest in the use of helminth infections to treat allergies and autoimmune diseases, exploiting their ability to induce immune hyporesponsiveness (8).Suppressed lymphocyte responses were described in the 19...

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confidence: 99%

“…Several regulatory cells and molecules are thought to play an important role in the regulatory network (3). Within T-cell responses, expansion of Tregulatory cells (Tregs) is reported in both animal models (10) and some human studies (11,12). Tregs suppress helminthspecific and bystander proliferative and proinflammatory responses.…”

mentioning

confidence: 99%

Community deworming alleviates geohelminth-induced immune hyporesponsiveness

Wammes

Hamid

Wiria

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…A proper antigen preparation, however, would be required for such study since larval immunodominant antigens might differ from those derived from adult worms. It also would be interesting to analyze in this context whether animal hookworm larvae may secrete proteins that interfere with the immune response and thereby promote survival as it has been shown for various other helminths [39,40].…”

Section: Discussionmentioning

confidence: 99%

Hookworm-related cutaneous larva migrans in patients living in an endemic community in Brazil: Immunological patterns before and after ivermectin treatment

Shimogawara¹,

Hata²,

Schuster³

et al. 2013

European Journal of Microbiology and Immunology

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Hookworm-related cutaneous larva migrans (Hr-CLM) is caused by animal hookworm larvae migrating in the human epidermis where they elicit an inflammatory response. This study describes the immunological profile in Hr-CLM patients.In 77 Hr-CLM patients from Manaus, Brazil, peripheral eosinophils were counted, and serum concentrations of total immunoglobulin E (IgE) and selected cytokines were determined by ELISA before and after treatment with ivermectin. Controls included patients' household members (endemic controls), non-endemic Brazilian and Japanese individuals.Eosinophil counts and total IgE in Hr-CLM patients were higher than in controls and correlated with disease severity. Concentrations of interleukin (IL)-4, IL-5, IL-6, and IL-10 were higher in Hr-CLM patients than in endemic controls (p < 0.001) while no differences were detected for interferon (IFN)-γ, tumor necrosis factor (TNF)-α, IL-1β, IL-2, or transforming growth factor (TGF)-β. Following ivermectin treatment, numbers of eosinophils and concentrations of IL-4, IL-5, and IL-10 decreased whereas IgE, IFN-γ, and TGF-β concentrations increased. The IL-5/IFN-γ ratio declined from 5.9 (interquartile range [IQR] 0.8-31.6) before to 0.1 (IQR 0.05-0.2; p = 0.001) after treatment.Thus, although an impact of other infections on the immune parameters determined cannot be excluded, Hr-CLM in endemic areas is associated with eosinophilia and elevated cytokine levels, particularly of IL-5 and IL-10, which decrease following ivermectin treatment.

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“…The immune response mounted to helminthic infections is characterized by T-helper type 2 (Th2), which is thought to be protective [4]. There is also evidence, however, that these parasites might enhance their own survival by modulating the immune responses of their host and inducing regulatory responses that dampen activity of effector cells [5].…”

Section: Introductionmentioning

confidence: 99%

“…Apart from the fact that Th2 response has evolved to minimize the virulence of helminthes [4], Th2 responses also protect against allergies and asthma, limit the number of helminths in the intestinal tract [13] and repair tis-sue damage caused by the helminths that have colonized the intestine [17]. In addition to the Th2 responses during helminthic infection regulatory B cells, alternatively activated macrophages (or M2) were key components of the immune regulatory network functioning during helminthic infections [18].…”

Section: Introductionmentioning

confidence: 99%

Intestinal Helminthic Infection Increases Serum Levels of IL-2 and Decreases Serum TGF-Beta Levels in Nigerian Asthmatic Patients

Arinola¹,

Oluwole²,

Oladokun³

et al. 2014

OJI

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Background: Asthma is less common in countries outside the organization for economic cooperation and development (OECD). One suggested mechanism for this disparity is the early life exposure to helminthic infection in non-OECD countries due to predominant Th1 immune response, which down-regulates Th2 responses required for exacerbation of asthma. This report is the first in the literature to describe the effects of helminthic infection on immune responses in asthmatic children compared to non-asthmatic controls. Methods: We administered the International Study of Asthma and Allergies in Childhood (ISAAC) questionnaire to 1690 high school students in three rural communities in southwestern Nigeria. Based on questionnaire responses and medical examination, identified asthma cases were matched with controls. Stool samples were collected from all subjects and screened for intestinal helminthic infection. The serum of 12 asthmatics and 12 non-asthmatics (6 with intestinal helminthic infection and 6 without intestinal helminthic infection in each group) were assayed for interleukin (

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Modulation of Specific and Allergy‐Related Immune Responses by Helminths

Cited by 52 publications

References 181 publications

Community deworming alleviates geohelminth-induced immune hyporesponsiveness

Community deworming alleviates geohelminth-induced immune hyporesponsiveness

Hookworm-related cutaneous larva migrans in patients living in an endemic community in Brazil: Immunological patterns before and after ivermectin treatment

Intestinal Helminthic Infection Increases Serum Levels of IL-2 and Decreases Serum TGF-Beta Levels in Nigerian Asthmatic Patients

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