The interaction of Schistosoma mansoni infection with diabetes mellitus and obesity in mice

Abstract Human schistosomiasis is one of the most prevalent parasitic diseases worldwide. Various host factors can affect the host–parasite interactions. Therefore, the aim of the present work was to determine the parasitological, histopathological, biochemical, and immunological status of Schistoso...

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Main Authors: Alaa S. Amer, Ahmad A. Othman, Lamees M. Dawood, Kholoud A. El-Nouby, Geoffrey N. Gobert, Dina M. Abou Rayia
Format: Article
Language:English
Published: Nature Portfolio 2023-06-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-023-36112-5
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author Alaa S. Amer
Ahmad A. Othman
Lamees M. Dawood
Kholoud A. El-Nouby
Geoffrey N. Gobert
Dina M. Abou Rayia
author_facet Alaa S. Amer
Ahmad A. Othman
Lamees M. Dawood
Kholoud A. El-Nouby
Geoffrey N. Gobert
Dina M. Abou Rayia
author_sort Alaa S. Amer
collection DOAJ
description Abstract Human schistosomiasis is one of the most prevalent parasitic diseases worldwide. Various host factors can affect the host–parasite interactions. Therefore, the aim of the present work was to determine the parasitological, histopathological, biochemical, and immunological status of Schistosoma mansoni-infected hosts with metabolic disorders to identify the underlying possible mechanisms of these comorbidities. The study animals were divided into four groups. Group I represented the control groups, namely, the normal control group, the S. mansoni-infected control group, and the noninfected type 1 diabetes (T1DM), type 2 diabetes (T2DM), and obesity groups. The mice of the other three groups underwent induction of T1DM (Group II), T2DM (Group III) and obesity (Group IV) before being infected with S. mansoni. All mice were subjected to body weight measurement, blood glucose and insulin assessment, parasitological evaluation of adult worm count, tissue egg count and intestinal oogram. Histopathological and immunohistochemical study using anti-glial fibrillary acidic protein (GFAP) in hepatic stellate cells (HSCs) and image analysis of Masson’s trichrome-stained liver sections using ImageJ (Fiji) software were carried out. Additionally, immunological analysis of tumour necrosis factor (TNF) beta, interleukin-5 (IL-5), IL-10, Forkhead box P3 (FOXP3) and pentraxin 3 (PTX3) levels besides biochemical study of total lipid profile were evaluated. The present study revealed a significant increase in the adult worm count and tissue egg output in the obesity group compared to the infected control group. The oogram of counted eggs showed prevalence of immature eggs in T1DM group, while T2DM and obese groups showed prevalence of mature eggs. The fibrosis area percentage showed significant increase in T2DM and obese groups while it was decreased in T1DM group in comparison to infected control group. Our data also showed significant increase in the levels of TNF-β, IL-5, PTX3 in T1DM, T2DM and obesity groups in comparison to infected control group, whilst the levels of FOXP3 and IL-10 were increased in the infected groups in comparison to their noninfected controls. Moreover, infected T1DM, T2DM and obesity groups showed higher blood glucose and lipid profile in comparison to the infected control group. However, these parameters were improved in comparison to their noninfected controls. In sum, induction of T2DM and obesity increased tissue egg counts, mature egg percentage, and fibrosis density, while schistosome infection induced changes in the lipid profile and blood glucose levels in infected diabetic and obese groups and impacted favorably insulin levels in obese mice. By better understanding the complexities of host–parasite interactions, efforts to reduce the burden of these debilitating diseases can be improved.
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spelling doaj.art-f4fb064816ef496e95e504299a2e93722023-06-11T11:12:00ZengNature PortfolioScientific Reports2045-23222023-06-0113111810.1038/s41598-023-36112-5The interaction of Schistosoma mansoni infection with diabetes mellitus and obesity in miceAlaa S. Amer0Ahmad A. Othman1Lamees M. Dawood2Kholoud A. El-Nouby3Geoffrey N. Gobert4Dina M. Abou Rayia5Medical Parasitology Department, Faculty of Medicine, Tanta UniversityMedical Parasitology Department, Faculty of Medicine, Tanta UniversityBiochemistry Department, Faculty of Medicine, Tanta UniversityMedical Parasitology Department, Faculty of Medicine, Tanta UniversitySchool of Biological Science, Institute for Global Food Security, Queen’s University BelfastMedical Parasitology Department, Faculty of Medicine, Tanta UniversityAbstract Human schistosomiasis is one of the most prevalent parasitic diseases worldwide. Various host factors can affect the host–parasite interactions. Therefore, the aim of the present work was to determine the parasitological, histopathological, biochemical, and immunological status of Schistosoma mansoni-infected hosts with metabolic disorders to identify the underlying possible mechanisms of these comorbidities. The study animals were divided into four groups. Group I represented the control groups, namely, the normal control group, the S. mansoni-infected control group, and the noninfected type 1 diabetes (T1DM), type 2 diabetes (T2DM), and obesity groups. The mice of the other three groups underwent induction of T1DM (Group II), T2DM (Group III) and obesity (Group IV) before being infected with S. mansoni. All mice were subjected to body weight measurement, blood glucose and insulin assessment, parasitological evaluation of adult worm count, tissue egg count and intestinal oogram. Histopathological and immunohistochemical study using anti-glial fibrillary acidic protein (GFAP) in hepatic stellate cells (HSCs) and image analysis of Masson’s trichrome-stained liver sections using ImageJ (Fiji) software were carried out. Additionally, immunological analysis of tumour necrosis factor (TNF) beta, interleukin-5 (IL-5), IL-10, Forkhead box P3 (FOXP3) and pentraxin 3 (PTX3) levels besides biochemical study of total lipid profile were evaluated. The present study revealed a significant increase in the adult worm count and tissue egg output in the obesity group compared to the infected control group. The oogram of counted eggs showed prevalence of immature eggs in T1DM group, while T2DM and obese groups showed prevalence of mature eggs. The fibrosis area percentage showed significant increase in T2DM and obese groups while it was decreased in T1DM group in comparison to infected control group. Our data also showed significant increase in the levels of TNF-β, IL-5, PTX3 in T1DM, T2DM and obesity groups in comparison to infected control group, whilst the levels of FOXP3 and IL-10 were increased in the infected groups in comparison to their noninfected controls. Moreover, infected T1DM, T2DM and obesity groups showed higher blood glucose and lipid profile in comparison to the infected control group. However, these parameters were improved in comparison to their noninfected controls. In sum, induction of T2DM and obesity increased tissue egg counts, mature egg percentage, and fibrosis density, while schistosome infection induced changes in the lipid profile and blood glucose levels in infected diabetic and obese groups and impacted favorably insulin levels in obese mice. By better understanding the complexities of host–parasite interactions, efforts to reduce the burden of these debilitating diseases can be improved.https://doi.org/10.1038/s41598-023-36112-5
spellingShingle Alaa S. Amer
Ahmad A. Othman
Lamees M. Dawood
Kholoud A. El-Nouby
Geoffrey N. Gobert
Dina M. Abou Rayia
The interaction of Schistosoma mansoni infection with diabetes mellitus and obesity in mice
Scientific Reports
title The interaction of Schistosoma mansoni infection with diabetes mellitus and obesity in mice
title_full The interaction of Schistosoma mansoni infection with diabetes mellitus and obesity in mice
title_fullStr The interaction of Schistosoma mansoni infection with diabetes mellitus and obesity in mice
title_full_unstemmed The interaction of Schistosoma mansoni infection with diabetes mellitus and obesity in mice
title_short The interaction of Schistosoma mansoni infection with diabetes mellitus and obesity in mice
title_sort interaction of schistosoma mansoni infection with diabetes mellitus and obesity in mice
url https://doi.org/10.1038/s41598-023-36112-5
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