Presence of intestinal helminths decreases T helper type 1 responses in tuberculoid leprosy patients and may increase the risk for multi-bacillary leprosy

Diniz, Lúcia Martins; Magalhaes, Eneida F. L.; Pereira, Fausto Edmundo Lima; Dietze, Reynaldo; Ribeiro‐Rodrigues, Rodrigo

doi:10.1111/j.1365-2249.2010.04164.x

Cited by 40 publications

(43 citation statements)

References 28 publications

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“…IFN-γ significantly decreases in the face of increased GI helminth infection intensity and increase after anthelminthic treatment [16]. Though our sample size was small and seasonal comparisons were nonsignificant, our approximately twofold decrease in mean IFN-γ signal in wet seasons when hosts were experiencing peak new GI helminth infections compared to in the relatively parasite-depleted dry season supports previous findings [15,16]. In addition, the significantly negative association between IFN-γ signal and animals with high GI parasite infections in conjunction with either high eosinophil counts or IgE titers lends support for opposing patterns between this Th1-type cytokine and parasites and parasite related immune factors, as would be expected in a parasite driven Th2-type immune skewing.…”

Section: Seasonal Immune Resource Allocationsupporting

confidence: 78%

“…The pathways leading to and from Th1-type responses and Th2-type responses are mutually cross-regulated; thus, hosts have difficulty simultaneously mounting effective Th1 and Th2 responses [11,12]. Many studies have demonstrated that helminth infections are particularly adept at skewing immune responses toward the Th2 arm [11,13] and downregulating Th1 immunity even in the face of microparasitic coinfections [6,9,[14][15][16]. Chronic helminth infections may also cause host immunosuppression, resulting in maintenance of the immunomodulating worm infection [17] and increased susceptibility to coinfections [18].…”

Section: Introductionmentioning

confidence: 99%

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Gastrointestinal helminths may affect host susceptibility to anthrax through seasonal immune trade-offs

et al. 2014

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Background: Most vertebrates experience coinfections, and many pathogen-pathogen interactions occur indirectly through the host immune system. These interactions are particularly strong in mixed micro-macroparasite infections because of immunomodulatory effects of helminth parasites. While these trade-offs have been examined extensively in laboratory animals, few studies have examined them in natural systems. Additionally, many wildlife pathogens fluctuate seasonally, at least partly due to seasonal host immune changes. We therefore examined seasonality of immune resource allocation, pathogen abundance and exposure, and interactions between infections and immunity in plains zebra (Equus quagga) in Etosha National Park (ENP), Namibia, a system with strongly seasonal patterns of gastrointestinal (GI) helminth infection intensity and concurrent anthrax outbreaks. Both pathogens are environmentally transmitted, and helminth seasonality is driven by environmental pressures on free living life stages. The reasons behind anthrax seasonality are currently not understood, though anthrax is less likely directly driven by environmental factors. Results: We measured a complex, interacting set of variables and found evidence that GI helminth infection intensities, eosinophil counts, IgE and IgGb antibody titers, and possibly IL-4 cytokine signaling were increased in wetter seasons, and that ectoparasite infestations and possibly IFN-γ cytokine signaling were increased in drier seasons. Monocyte counts and anti-anthrax antibody titers were negatively associated with wet season eosinophilia, and monocytes were negatively correlated with IgGb and IgE titers. Taken together, this supports the hypothesis that ENP wet seasons are characterized by immune resource allocation toward Th-2 type responses, while Th1-type immunity may prevail in drier seasons, and that hosts may experience Th1-Th2 trade-offs. We found evidence that this Th2-type resource allocation is likely driven by GI parasite infections, and that these trade-offs may render hosts less capable of concurrently mounting effective Th1-type immune responses against anthrax. Conclusions: This study is one of the first to examine laboratory-demonstrated Th1-Th2 trade-offs in a natural system. It provides evidence that seasonally bound pathogens may affect, through immunology, transmission dynamics of pathogens that might otherwise not be seasonally distributed. It suggests that, by manipulating the internal host ecosystem, GI parasites may influence the external ecosystem by affecting the dynamics of another environmentally transmitted pathogen.

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Section: Seasonal Immune Resource Allocationsupporting

confidence: 78%

Section: Introductionmentioning

confidence: 99%

Gastrointestinal helminths may affect host susceptibility to anthrax through seasonal immune trade-offs

et al. 2014

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“…34 Other studies have examined the effect of A lumbricoides infection on immunologic responses and outcomes among a cohort of patients with leprosy, another mycobacterial disease that depends on intact Th1 responses for control. 35 In comparison to patients with leprosy alone, those who were coinfected with intestinal helminths were more likely to have severe forms of leprosy and lower levels of IFN-γ. A mechanism that potentially explains helminth infection–related alterations in T-cell responses can be found from a study 11 that compared the immune activation status and cellular responses to purified protein derivative among people with and without chronic helminth infections from TB-endemic areas.…”

Section: Discussionmentioning

confidence: 96%

Malnutrition and Helminth Infection Affect Performance of an Interferon γ–Release Assay

et al. 2010

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OBJECTIVE We sought to compare the tuberculin skin test (TST) to the QuantiFERON-TB Gold In-Tube assay (QFT-IT) and assess the effects of malnourishment and intestinal helminth infection on QFT-IT results. METHODS In this population-based cross-sectional study from Dhaka, Bangladesh, we screened children for latent tuberculosis infection with the QFT-IT and TST. We assess the agreement between the TST and QFT-IT, risk factors associated with indeterminate QFT-IT results, and magnitude of interferon γ (IFN-γ) production. RESULTS Three hundred and two children (aged 11–15.3 years) were enrolled, including 93 (30.8%) who were malnourished. Of 251 participants who provided stool samples, 117 (46.6%) were infected with Ascaris lumbricoides and/or Trichuris trichiura. TST results were positive (≥10 mm) for 101 (33.4%) children and negative for 201 (66.6%) children. QFT-IT results were positive for 107 (35.4%) children, negative for 121 (40.1%) children, and indeterminate for 74 (24.5%) children. Agreement between the tests was moderate (κ = 0.55 [95% confidence interval: 0.44–0.65]; P < .0001) when excluding indeterminate results. Children with indeterminate QFT-IT results were separately compared with children with positive and negative QFT-IT results; malnutrition (P = .0006 and .0003), and helminth infection (P = .05 and .02), and the statistical interaction between these 2 terms (P = .03 and .004) were associated with indeterminate results. Higher levels of IFN-γ in response to tuberculosis antigens were associated with positive TST results (P < .0001); lower levels were associated with malnutrition (P = .02). CONCLUSIONS Malnutrition and helminth infections were associated with indeterminate QFT-IT results. Therefore, the presence of such conditions may limit the interpretability of QFT-IT results in children.

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“…An association between intestinal helminth infections and lepromatous leprosy has been demonstrated with the frequency of intestinal helminths correlating strongly with the mycobacterial index [Diniz et al, 2010]. Evidence that Th1 downmodulation occurs during intestinal helminth infection was provided by the fact that intracellular IFN-g levels in both tuberculoid and lepromatous, helminth free leprosy patients, were approximately 2-fold higher than in helminth infected leprosy patients.…”

mentioning

confidence: 97%

“…Conversely, lepromatous patients harboring intestinal helminths produced close to 2-fold more IL-4 and IL-10 than helminth-free leprosy patients. These results suggest that a pre-existing infection by intestinal helminths may facilitate initial M. leprae infection or its progression to a more severe clinical form [Diniz et al, 2010].…”

mentioning

confidence: 98%

Clinical, immunological, and genetic aspects in leprosy

Simon

Scherlock

Duthie

et al. 2011

Drug Development Research

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Leprosy is a chronic infection caused by Mycobacterium leprae. It affects the skin and peripheral nerves and can cause irreversible chronic disabilities. The worldwide registered number of cases in 2009 was 213,036. This review discusses clinical aspects of the disease, including leprosy reactions and neuronal damage, as well as immunological and immunogenetic aspects influencing disease susceptibility and outcome. The cardinal signs of leprosy are skin lesions with altered sensation, thickened peripheral nerves, and presence of alcohol acid-resistant bacilli in skin biopsy or lymph. Confirmatory examinations include (1) bacteriological examination, which allows patients' classification into two operational groups, multibacillary (MB) and paucibacillary (PB); and (2) histopathological examination, which permits stratification in different clinical forms. These clinical forms differ not only by histopathology but also according to the host's immune response to M. leprae. These forms comprise the extremes of (1) tuberculoid leprosy (TT), with a specific Th1 response and control of M. leprae multiplication; (2) lepromatous leprosy (LL) without Th1 response and preserved Th2 response; and (3) the interpolar clinical forms, borderline tuberculoid (BT), borderline borderline (BB), borderline lepromatous (BL), and indeterminate form (IL). Appropriate treatment is based on smear examination or the number of lesions at diagnosis. In the evolution of leprosy, acute inflammation, known as reactions, may occur during or after treatment. These reactions are classified into two main types: the type I reaction or reversal reaction (RR), and the type II reaction or erythema nodosum leprosum (ENL). The role of innate immune response to control the infection is supported by immunological and genetic studies. Drug Dev Res 72:509-527, 2011.

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Presence of intestinal helminths decreases T helper type 1 responses in tuberculoid leprosy patients and may increase the risk for multi-bacillary leprosy

Cited by 40 publications

References 28 publications

Gastrointestinal helminths may affect host susceptibility to anthrax through seasonal immune trade-offs

Gastrointestinal helminths may affect host susceptibility to anthrax through seasonal immune trade-offs

Malnutrition and Helminth Infection Affect Performance of an Interferon γ–Release Assay

Clinical, immunological, and genetic aspects in leprosy

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