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Atopy Is Inversely Related to Schistosome Infection Intensity: A Comparative Study in Zimbabwean Villages with Distinct Levels of Schistosoma haematobium Infection

Rujeni, Nadine, Nausch, Norman, Bourke, Claire D., Midzi, Nicholas, Mduluza, Takafira, Taylor, David W., Mutapi, Francisca·2012·International Archives of Allergy and Immunology

Abstract

Background: The hygiene hypothesis suggests that parasitic infections protect against allergic diseases by modulating the host’s immune responses. Experimental studies indicate that this protection depends on the intensity of parasitic infection, but this observation has not been tested in human populations. The aim of this study is to investigate whether the intensity of Schistosoma haematobium infection is related to atopic responses and whether this relationship differs between populations with distinct parasite transmission dynamics. Methods: The study was conducted in two villages with different Schistosoma haematobium transmission dynamics, i.e. high (n = 365) and low (n = 307) transmission. Allergic reactivity to the common house dust mite (Dermatophagoides pteronyssinus) was measured by skin prick tests and allergen-specific IgE and IgG4 quantified by enzyme-linked immunosorbent assay. Atopic responses were related to current infection intensity and schistosome transmission levels. Results: Schistosome infection intensity was negatively associated with the skin prick reactivity, mite-specific IgE and the ratio IgE/IgG4 in the high-transmission village. However, when only low levels of infection were analyzed in the 2 villages, there was no correlation between mite-specific responses and infection intensity. Conclusion: The relationship between schistosome infection and atopic responses is dependent on the intensity of current schistosome infection. Thus, consistent with results from animal models, with an increasing parasite burden, the immunoregulation of immune responses to allergens appears to become more pronounced.

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Fig. 1 Prevalence and infection intensity according to age in the study area. Infection intensity (a) and prevalence (b) are plotted against age groups in the high-transmission (– – –) and the low-transmission area (––––). Bars represent standard error of the means for infection intensity and 95% CI for the prevalence. * p < 0.05 and ** p < 0.01 represent significant differences in each group between the two villages.
Fig. 1 Prevalence and infection intensity according to age in the study area. Infection intensity (a) and prevalence (b) are plotted against age groups in the high-transmission (– – –) and the low-transmission area (––––). Bars represent standard error of the means for infection intensity and 95% CI for the prevalence. * p < 0.05 and ** p < 0.01 represent significant differences in each group between the two villages.CC BY-NC · PubMed Central
Fig. 2 Antibody levels according to age. Der p 1-specific, SWAP-specific and SEA-specific responses in the high-transmission (– – –) and the low-transmission area (––––). Bars represent standard error of the means. * p < 0.05 and ** p < 0.01 represent significant differences in each group between the two villages.
Fig. 2 Antibody levels according to age. Der p 1-specific, SWAP-specific and SEA-specific responses in the high-transmission (– – –) and the low-transmission area (––––). Bars represent standard error of the means. * p < 0.05 and ** p < 0.01 represent significant differences in each group between the two villages.CC BY-NC · PubMed Central
Fig. 3 Der p 1-specific antibody levels in SPT-positive versus SPT-negative individuals. Levels (absorbencies) of anti-Der p 1 IgE and IgG4 are plotted for SPT-negative and SPT-positive people. Bars represent standard error of the means. n.s. = Difference not significant, versus ** p < 0.01 = a significant difference.
Fig. 3 Der p 1-specific antibody levels in SPT-positive versus SPT-negative individuals. Levels (absorbencies) of anti-Der p 1 IgE and IgG4 are plotted for SPT-negative and SPT-positive people. Bars represent standard error of the means. n.s. = Difference not significant, versus ** p < 0.01 = a significant difference.CC BY-NC · PubMed Central
Fig. 4 Correlation between SPT results and infection intensity. Residuals of infection intensity after controlling for age, sex and village of residence are plotted against the size of the wheal in millimeters.
Fig. 4 Correlation between SPT results and infection intensity. Residuals of infection intensity after controlling for age, sex and village of residence are plotted against the size of the wheal in millimeters.CC BY-NC · PubMed Central
Fig. 5 Correlations between schistosome-specific:mite-specific antibody ratio and infection intensity. Residuals (after controlling for age and sex) of IgE, IgG4 and IgE/IgG4 against Der p 1 (a), SWAPs (b) and SEAs (c) are plotted against infection intensity (log-transformed) for Magaya (high-transmission area) and Chitate (low-transmission area). One-tailed Pearson correlations were performed. Correlations significant at p < 0.05 are highlighted in bold. Resid = Residual.
Fig. 5 Correlations between schistosome-specific:mite-specific antibody ratio and infection intensity. Residuals (after controlling for age and sex) of IgE, IgG4 and IgE/IgG4 against Der p 1 (a), SWAPs (b) and SEAs (c) are plotted against infection intensity (log-transformed) for Magaya (high-transmission area) and Chitate (low-transmission area). One-tailed Pearson correlations were performed. Correlations significant at p < 0.05 are highlighted in bold. Resid = Residual.CC BY-NC · PubMed Central

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Metadata

Authors
Rujeni, N., Nausch, N., Bourke, C. D., Midzi, N., Mduluza, T., Taylor, D. W., & Mutapi, F.
Venue
International Archives of Allergy and Immunology
Publisher
S. Karger AG
Published
2012
Volume
158
Issue
3
Pages
288-298
ISSN
  • 1018-2438
  • 1423-0097
Cited by
47
References
0
Language
en

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