Asmaa M El-Kady, Sarah A Altwaim, Majed H Wakid, Alaa S Banjar, Khalil Mohammed, Mashael S Alfaifi, Hayam Elshazly, Wafa Abdullah I Al-Megrin, Eman Abdullah Alshehri, Eman Sayed, Hatem A Elshabrawy
{"title":"Prior <i>Trichinella spiralis</i> infection protects against <i>Schistosoma mansoni</i> induced hepatic fibrosis.","authors":"Asmaa M El-Kady, Sarah A Altwaim, Majed H Wakid, Alaa S Banjar, Khalil Mohammed, Mashael S Alfaifi, Hayam Elshazly, Wafa Abdullah I Al-Megrin, Eman Abdullah Alshehri, Eman Sayed, Hatem A Elshabrawy","doi":"10.3389/fvets.2024.1443267","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Schistosomiasis affects approximately 250 million people worldwide, with 200,000 deaths annually. It has been documented that the granulomatous response to <i>Schistosoma mansoni</i> (<i>S. mansoni</i>) oviposition is the root cause of progressive liver fibrosis in chronic infection, in 20% of the patients, and can lead to liver cirrhosis and/or liver cancer. The influence of helminths coinfection on schistosomiasis-induced liver pathological alterations remains poorly understood. Therefore, in this study, we investigated the effect of <i>Trichinella spiralis</i> (<i>T. spiralis</i>) infection on <i>S. mansoni</i>-induced hepatic fibrosis.</p><p><strong>Materials and methods: </strong>Thirty adult male Balb-c mice were divided into three groups. Group 1 was left uninfected; group 2 was infected with <i>S. mansoni</i> cercariae and group 3 was orally infected with <i>T. spiralis</i> larvae, then 28 days later, this group was infected with <i>S. mansoni</i> cercariae. All groups were sacrificed at the end of the 8<sup>th</sup> week post infection with <i>S. mansoni to evaluate</i> the effect of pre-infection with <i>T. spiralis</i> on <i>S. mansoni</i> induced liver fibrosis was evaluated parasitologically (worm burden and egg count in tissues), biochemically (levels of alanine aminotransferase and aspartate aminotransferase), histopathologically (H&E and MT staining, and immunohistochemical staining for the expression of α-SMA, IL-6, IL-1β, IL-17, IL-23, TNF-α, and TGF-β).</p><p><strong>Results: </strong>The results in the present study demonstrated marked protective effect of <i>T. spiralis</i> against <i>S. mansoni</i> induced liver pathology. We demonstrated that pre-infection with <i>T. spirais</i> caused marked reduction in the number of <i>S. mansoni</i> adult worms (3.17 ± 0.98 vs. 18 ± 2.16, <i>P</i> = 0.114) and egg count in both the intestine (207.2 ± 64.3 vs. 8,619.43 ± 727.52, <i>P</i> = 0.009) and liver tissues (279 ± 87.2 vs. 7,916.86 ± 771.34; <i>P</i> = 0.014). Consistently, we found significant reductions in both number (3.4 ± 1.1 vs. 11.8.3 ± 1.22; <i>P</i> = 0.007) and size (84 ± 11 vs. 294.3 ± 16.22; <i>P</i> = 0.001) of the hepatic granulomas in mice pre-infected with <i>T. spiralis</i> larvae compared to those infected with only <i>S. mansoni</i>. Furthermore, pre- infection with <i>T. spiralis</i> markedly reduced <i>S. mansoni</i>- induced hepatic fibrosis, as evidenced by decreased collagen deposition, low expression of α-SMA, and significantly reduced levels of IL-17, IL-1B, IL-6, TGF-B, IL-23, and TNF-α compared to mice infected with <i>S. mansoni</i> only.</p><p><strong>Conclusions: </strong>Our data show that pre-infection with <i>T. spiralis</i> effectively protected mice from severe schistosomiasis and liver fibrosis. We believe that our findings support the potential utility of helminths for the preventing and ameliorating severe pathological alterations induced by schistosomiasis.</p>","PeriodicalId":12772,"journal":{"name":"Frontiers in Veterinary Science","volume":null,"pages":null},"PeriodicalIF":2.6000,"publicationDate":"2024-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11494294/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Frontiers in Veterinary Science","FirstCategoryId":"97","ListUrlMain":"https://doi.org/10.3389/fvets.2024.1443267","RegionNum":2,"RegionCategory":"农林科学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/1/1 0:00:00","PubModel":"eCollection","JCR":"Q1","JCRName":"VETERINARY SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Background: Schistosomiasis affects approximately 250 million people worldwide, with 200,000 deaths annually. It has been documented that the granulomatous response to Schistosoma mansoni (S. mansoni) oviposition is the root cause of progressive liver fibrosis in chronic infection, in 20% of the patients, and can lead to liver cirrhosis and/or liver cancer. The influence of helminths coinfection on schistosomiasis-induced liver pathological alterations remains poorly understood. Therefore, in this study, we investigated the effect of Trichinella spiralis (T. spiralis) infection on S. mansoni-induced hepatic fibrosis.
Materials and methods: Thirty adult male Balb-c mice were divided into three groups. Group 1 was left uninfected; group 2 was infected with S. mansoni cercariae and group 3 was orally infected with T. spiralis larvae, then 28 days later, this group was infected with S. mansoni cercariae. All groups were sacrificed at the end of the 8th week post infection with S. mansoni to evaluate the effect of pre-infection with T. spiralis on S. mansoni induced liver fibrosis was evaluated parasitologically (worm burden and egg count in tissues), biochemically (levels of alanine aminotransferase and aspartate aminotransferase), histopathologically (H&E and MT staining, and immunohistochemical staining for the expression of α-SMA, IL-6, IL-1β, IL-17, IL-23, TNF-α, and TGF-β).
Results: The results in the present study demonstrated marked protective effect of T. spiralis against S. mansoni induced liver pathology. We demonstrated that pre-infection with T. spirais caused marked reduction in the number of S. mansoni adult worms (3.17 ± 0.98 vs. 18 ± 2.16, P = 0.114) and egg count in both the intestine (207.2 ± 64.3 vs. 8,619.43 ± 727.52, P = 0.009) and liver tissues (279 ± 87.2 vs. 7,916.86 ± 771.34; P = 0.014). Consistently, we found significant reductions in both number (3.4 ± 1.1 vs. 11.8.3 ± 1.22; P = 0.007) and size (84 ± 11 vs. 294.3 ± 16.22; P = 0.001) of the hepatic granulomas in mice pre-infected with T. spiralis larvae compared to those infected with only S. mansoni. Furthermore, pre- infection with T. spiralis markedly reduced S. mansoni- induced hepatic fibrosis, as evidenced by decreased collagen deposition, low expression of α-SMA, and significantly reduced levels of IL-17, IL-1B, IL-6, TGF-B, IL-23, and TNF-α compared to mice infected with S. mansoni only.
Conclusions: Our data show that pre-infection with T. spiralis effectively protected mice from severe schistosomiasis and liver fibrosis. We believe that our findings support the potential utility of helminths for the preventing and ameliorating severe pathological alterations induced by schistosomiasis.
期刊介绍:
Frontiers in Veterinary Science is a global, peer-reviewed, Open Access journal that bridges animal and human health, brings a comparative approach to medical and surgical challenges, and advances innovative biotechnology and therapy.
Veterinary research today is interdisciplinary, collaborative, and socially relevant, transforming how we understand and investigate animal health and disease. Fundamental research in emerging infectious diseases, predictive genomics, stem cell therapy, and translational modelling is grounded within the integrative social context of public and environmental health, wildlife conservation, novel biomarkers, societal well-being, and cutting-edge clinical practice and specialization. Frontiers in Veterinary Science brings a 21st-century approach—networked, collaborative, and Open Access—to communicate this progress and innovation to both the specialist and to the wider audience of readers in the field.
Frontiers in Veterinary Science publishes articles on outstanding discoveries across a wide spectrum of translational, foundational, and clinical research. The journal''s mission is to bring all relevant veterinary sciences together on a single platform with the goal of improving animal and human health.