Mechanisms and clinical relevance of the bidirectional relationship of viral infections with metabolic diseases

Nikolaos Perakakis¹, Hani Harb², Benjamin G Hale³, Zsuzsanna Varga⁴, Charlotte Steenblock⁵, Waldemar Kanczkowski⁵, Vasileia Ismini Alexaki⁶, Barbara Ludwig⁷, Peter Mirtschink⁶, Michele Solimena⁸, Nicole Toepfner⁹, Sebastian Zeissig¹⁰, Manuel Gado¹¹, Irene Alma Abela¹², Felix Beuschlein¹³, Giatgen A Spinas¹⁴, Claudia Cavelti-Weder¹⁴, Philipp A Gerber¹⁴, Michael Huber³, Alexandra Trkola³, Milo A Puhan¹⁵, Wendy Wei-Lynn Wong¹⁶, Andreas Linkermann¹⁷, Viswanathan Mohan¹⁸, Hendrik Lehnert¹⁹, Peter Nawroth⁵, Triantafyllos Chavakis²⁰, Geltrude Mingrone²¹, Christian Wolfrum²², Annelies S Zinkernagel²³, Stefan R Bornstein²⁴

Affiliations

¹ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany. Electronic address: Nikolaos.Perakakis@uniklinikum-dresden.de.
² Medical Microbiology and Virology, Technische Universität Dresden, Dresden 01307, Germany.
³ Institute of Medical Virology, University of Zürich, Zürich, Switzerland.
⁴ Department of Pathology and Molecular Pathology, University of Zürich, Zürich, Switzerland.
⁵ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany.
⁶ Institute for Institute of Clinical Chemistry and Laboratory Medicine, Technische Universität Dresden, Dresden 01307, Germany.
⁷ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany.
⁸ Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; Department of Molecular Diabetology, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany.
⁹ Department of Pediatrics, Technische Universität Dresden, Dresden 01307, Germany.
¹⁰ Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden 01307, Germany; Department of Medicine I, Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden 01307, Germany.
¹¹ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany.
¹² Institute of Medical Virology, University of Zürich, Zürich, Switzerland; Department of Infectious Diseases and Hospital Epidemiology, University of Zürich, Zürich, Switzerland.
¹³ Department of Endocrinology, Diabetology and Clinical Nutrition, University Hospital Zürich, University of Zürich, Zürich, Switzerland; Medizinische Klinik und Poliklinik IV, Klinikum der Universität, Ludwig-Maximilians-Universität München, Munich, Germany.
¹⁴ Department of Endocrinology, Diabetology and Clinical Nutrition, University Hospital Zürich, University of Zürich, Zürich, Switzerland.
¹⁵ Epidemiology, Biostatistics and Prevention Institute, University of Zürich, Zürich, Switzerland.
¹⁶ and Department of Molecular Life Science, University of Zürich, Zürich, Switzerland.
¹⁷ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Division of Nephrology, Department of Medicine, Albert Einstein College of Medicine, Bronx, New York, USA.
¹⁸ Madras Diabetes Research Foundation and Dr. Mohan's Diabetes Specialties Centre, Chennai, Tamil Nadu, India.
¹⁹ Presidential Office, Paris Lodron Universität Salzburg, Salzburg, Austria.
²⁰ Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; Institute for Institute of Clinical Chemistry and Laboratory Medicine, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany; Centre for Cardiovascular Science, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.
²¹ Department of Translational Medicine and Surgery, Università Cattolica del Sacro Cuore, Rome, Italy; Department of Medical and Surgical Sciences, Fondazione Policlinico Universitario A Gemelli IRCCS, Rome, Italy; Division of Diabetes and Nutritional Sciences, School of Cardiovascular and Metabolic Medicine and Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.
²² Laboratory of Translational Nutrition Biology, Institute of Food, Nutrition and Health, Department of Health Sciences and Technology, ETH Zürich, Schwerzenbach, Switzerland.
²³ Department of Infectious Diseases and Hospital Epidemiology, University of Zürich, Zürich, Switzerland.
²⁴ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany; Division of Diabetes and Nutritional Sciences, School of Cardiovascular and Metabolic Medicine and Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.

PMID: 37524103
DOI: 10.1016/S2213-8587(23)00154-7

Review

Mechanisms and clinical relevance of the bidirectional relationship of viral infections with metabolic diseases

Nikolaos Perakakis et al. Lancet Diabetes Endocrinol. 2023 Sep.

. 2023 Sep;11(9):675-693.

doi: 10.1016/S2213-8587(23)00154-7. Epub 2023 Jul 28.

Authors

Affiliations

¹ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany. Electronic address: Nikolaos.Perakakis@uniklinikum-dresden.de.
² Medical Microbiology and Virology, Technische Universität Dresden, Dresden 01307, Germany.
³ Institute of Medical Virology, University of Zürich, Zürich, Switzerland.
⁴ Department of Pathology and Molecular Pathology, University of Zürich, Zürich, Switzerland.
⁵ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany.
⁶ Institute for Institute of Clinical Chemistry and Laboratory Medicine, Technische Universität Dresden, Dresden 01307, Germany.
⁷ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany.
⁸ Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; Department of Molecular Diabetology, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany.
⁹ Department of Pediatrics, Technische Universität Dresden, Dresden 01307, Germany.
¹⁰ Center for Regenerative Therapies Dresden, Technische Universität Dresden, Dresden 01307, Germany; Department of Medicine I, Faculty of Medicine and University Hospital Carl Gustav Carus, Technische Universität Dresden, Dresden 01307, Germany.
¹¹ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany.
¹² Institute of Medical Virology, University of Zürich, Zürich, Switzerland; Department of Infectious Diseases and Hospital Epidemiology, University of Zürich, Zürich, Switzerland.
¹³ Department of Endocrinology, Diabetology and Clinical Nutrition, University Hospital Zürich, University of Zürich, Zürich, Switzerland; Medizinische Klinik und Poliklinik IV, Klinikum der Universität, Ludwig-Maximilians-Universität München, Munich, Germany.
¹⁴ Department of Endocrinology, Diabetology and Clinical Nutrition, University Hospital Zürich, University of Zürich, Zürich, Switzerland.
¹⁵ Epidemiology, Biostatistics and Prevention Institute, University of Zürich, Zürich, Switzerland.
¹⁶ and Department of Molecular Life Science, University of Zürich, Zürich, Switzerland.
¹⁷ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Division of Nephrology, Department of Medicine, Albert Einstein College of Medicine, Bronx, New York, USA.
¹⁸ Madras Diabetes Research Foundation and Dr. Mohan's Diabetes Specialties Centre, Chennai, Tamil Nadu, India.
¹⁹ Presidential Office, Paris Lodron Universität Salzburg, Salzburg, Austria.
²⁰ Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; Institute for Institute of Clinical Chemistry and Laboratory Medicine, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany; Centre for Cardiovascular Science, Queen's Medical Research Institute, University of Edinburgh, Edinburgh, UK.
²¹ Department of Translational Medicine and Surgery, Università Cattolica del Sacro Cuore, Rome, Italy; Department of Medical and Surgical Sciences, Fondazione Policlinico Universitario A Gemelli IRCCS, Rome, Italy; Division of Diabetes and Nutritional Sciences, School of Cardiovascular and Metabolic Medicine and Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.
²² Laboratory of Translational Nutrition Biology, Institute of Food, Nutrition and Health, Department of Health Sciences and Technology, ETH Zürich, Schwerzenbach, Switzerland.
²³ Department of Infectious Diseases and Hospital Epidemiology, University of Zürich, Zürich, Switzerland.
²⁴ Department of Internal Medicine III, Technische Universität Dresden, Dresden 01307, Germany; Paul Langerhans Institute Dresden, Helmholtz Munich, Technische Universität Dresden, Dresden 01307, Germany; German Center for Diabetes Research, Neuherberg, Germany; Division of Diabetes and Nutritional Sciences, School of Cardiovascular and Metabolic Medicine and Sciences, Faculty of Life Sciences and Medicine, King's College London, London, UK.

PMID: 37524103
DOI: 10.1016/S2213-8587(23)00154-7

Abstract

Viruses have been present during all evolutionary steps on earth and have had a major effect on human history. Viral infections are still among the leading causes of death. Another public health concern is the increase of non-communicable metabolic diseases in the last four decades. In this Review, we revisit the scientific evidence supporting the presence of a strong bidirectional feedback loop between several viral infections and metabolic diseases. We discuss how viruses might lead to the development or progression of metabolic diseases and conversely, how metabolic diseases might increase the severity of a viral infection. Furthermore, we discuss the clinical relevance of the current evidence on the relationship between viral infections and metabolic disease and the present and future challenges that should be addressed by the scientific community and health authorities.

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Conflict of interest statement

Declaration of interests NP reports consulting fees from Bayer Vital GmbH, speaker honoraria and travel support from Novo Nordisk, and speaker honoraria from GWT outside the submitted work. BGH is a member of the Gene Therapy Working Group, a permanent working group of the Swiss Expert Committee for Biosafety. NT is a member of the steering committee of the German Society for Pediatric Infectious Diseases. IAA reports grants from the Promedica foundation, consulting fees from Sanofi, speaker honoraria from MSD, and travel support from Gilead. PAG reports consulting fees and travel support from Novo Nordisk, consulting fees from Amgen, speaker honoraria from Eli Lilly, and is the President of the Swiss Association for the Study of Metabolism and Obesity. GM reports consulting fees from Novo Nordisk and Fractyl Health; participates on a data safety monitoring board or advisory board at Novo Nordisk, Fractyl Health, Recor, Metadeq, Keyron, and GHP Scientific; reports grants from Boehringer Ingelheim, and receives advisory board and speaker honoraria from Novo Nordisk and Boehringer Ingelheim. TC received grants from the European Research Council, Deutsche Forschungsgemeinschaft, US National Institutes of Health, Else Kröner Fresenius Center for Digital Health Dresden, Bundesministerium für Bildung und Forschung, German Center for Diabetes Research, and Sächsisches Staatsministerium für Wissenschaft, Kultur und Tourismus. All other authors report no competing interests.

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Mechanisms and clinical relevance of the bidirectional relationship of viral infections with metabolic diseases

Affiliations

Mechanisms and clinical relevance of the bidirectional relationship of viral infections with metabolic diseases

Authors

Affiliations

Abstract

Conflict of interest statement

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LinkOut - more resources

Full Text Sources

Medical