Changing our view of the Schistosoma granuloma to an ecological standpoint

ABSTRACT Schistosomiasis, a neglected parasitic tropical disease that has plagued humans for centuries, remains a major public health burden. A primary challenge to understanding schistosomiasis is deciphering the most remarkable pathological feature of this disease, the granuloma – a highly dynamic...

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Bibliographic Details
Published in:Biological reviews of the Cambridge Philosophical Society 2021-08, Vol.96 (4), p.1404-1420
Main Authors: Malta, Kássia K., Silva, Thiago P., Palazzi, Cinthia, Neves, Vitor H., Carmo, Lívia A. S., Cardoso, Simone J., Melo, Rossana C. N.
Format: Article
Language:English
Subjects:
Antigens
cellular ecology
Chemical compounds
Colonization
Cytokines
Ecological succession
Ecology
ecosystem
Ecosystems
Fibers
Granuloma
Granulomas
host–parasite interaction
Liver
Microenvironments
neglected tropical diseases
Parasites
Parasitic diseases
Populations
Public health
Schistosoma mansoni
Schistosomiasis
Structural hierarchy
Tropical diseases
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Summary:ABSTRACT Schistosomiasis, a neglected parasitic tropical disease that has plagued humans for centuries, remains a major public health burden. A primary challenge to understanding schistosomiasis is deciphering the most remarkable pathological feature of this disease, the granuloma – a highly dynamic and self‐organized structure formed by both host and parasite components. Granulomas are considered a remarkable example of how parasites evolved with their hosts to establish complex and intimate associations. However, much remains unclear regarding life within the granuloma, and strategies to restrain its development are still lacking. Here we explore current information on the hepatic Schistosoma mansoni granuloma in the light of Ecology and propose that this intricate structure acts as a real ecosystem. The schistosomal granuloma is formed by cells (biotic component), protein scaffolds, fibres, and chemical compounds (abiotic components) with inputs/outputs of energy and matter, as complex as in classical ecosystems. We review the distinct cell populations (‘species’) within the granuloma and examine how they integrate with each other and interact with their microenvironment to form a multifaceted cell community in different space–time frames. The colonization of the hepatic tissue to form granulomas is explained from the point of view of an ecological succession whereby a community is able to modify its physical environment, creating conditions and resources for ecosystem construction. Remarkably, the granuloma represents a dynamic evolutionary system that undergoes progressive changes in the ‘species’ that compose its community over time. In line with ecological concepts, we examine the granuloma not only as a place where a community of cells is settled (spatial niche or habitat) but also as a site in which the functional activities of these combined populations occur in an orchestrated way in response to microenvironmental gradients such as cytokines and egg antigens. Finally, we assert how the levels of organization of cellular components in a granuloma as conventionally defined by Cell Biology can fit perfectly into a hierarchical structure of biological systems as defined by Ecology. By rethinking the granuloma as an integrating and evolving ecosystem, we draw attention to the inner workings of this structure that are central to the understanding of schistosomiasis and could guide its future treatment.
ISSN:1464-7931
1469-185X
DOI:10.1111/brv.12708