Frontiers in Immunology (Jul 2024)
The longitudinal characterization of immune responses in COVID-19 patients reveals novel prognostic signatures for disease severity, patients’ survival and long COVID
- Maddalena Noviello,
- Maddalena Noviello,
- Rebecca De Lorenzo,
- Rebecca De Lorenzo,
- Raniero Chimienti,
- Norma Maugeri,
- Claudia De Lalla,
- Gabriel Siracusano,
- Nicola Ivan Lorè,
- Paola Maria Vittoria Rancoita,
- Federica Cugnata,
- Elena Tassi,
- Elena Tassi,
- Stefania Dispinseri,
- Danilo Abbati,
- Valeria Beretta,
- Valeria Beretta,
- Eliana Ruggiero,
- Francesco Manfredi,
- Aurora Merolla,
- Aurora Merolla,
- Elisa Cantarelli,
- Cristina Tresoldi,
- Claudia Pastori,
- Roberta Caccia,
- Francesca Sironi,
- Ilaria Marzinotto,
- Fabio Saliu,
- Silvia Ghezzi,
- Vito Lampasona,
- Elisa Vicenzi,
- Paola Cinque,
- Angelo Andrea Manfredi,
- Gabriella Scarlatti,
- Paolo Dellabona,
- Lucia Lopalco,
- Clelia Di Serio,
- Mauro Malnati,
- Fabio Ciceri,
- Fabio Ciceri,
- Patrizia Rovere-Querini,
- Patrizia Rovere-Querini,
- Chiara Bonini,
- Chiara Bonini,
- Chiara Bonini
Affiliations
- Maddalena Noviello
- Experimental Hematology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Maddalena Noviello
- Cell Therapy Immunomonitoring Laboratory Monitoraggio Immunologico Terapie Cellulari (MITiCi), Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Rebecca De Lorenzo
- Vita-Salute San Raffaele University, Milan, Italy
- Rebecca De Lorenzo
- Internal Medicine Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Raniero Chimienti
- Viral Evolution and Transmission Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Norma Maugeri
- Autoimmunity and Vascular Inflammation Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Claudia De Lalla
- Experimental Immunology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Gabriel Siracusano
- Immunobiology of Human Immunodeficiency Virus (HIV) Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Nicola Ivan Lorè
- Emerging Bacterial Pathogens Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Paola Maria Vittoria Rancoita
- 0University Centre for Statistics in the Biomedical Sciences (CUSSB), Vita-Salute San Raffaele University, Milan, Italy
- Federica Cugnata
- 0University Centre for Statistics in the Biomedical Sciences (CUSSB), Vita-Salute San Raffaele University, Milan, Italy
- Elena Tassi
- Experimental Hematology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Elena Tassi
- Cell Therapy Immunomonitoring Laboratory Monitoraggio Immunologico Terapie Cellulari (MITiCi), Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Stefania Dispinseri
- Viral Evolution and Transmission Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Danilo Abbati
- Experimental Hematology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Valeria Beretta
- Experimental Hematology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Valeria Beretta
- Cell Therapy Immunomonitoring Laboratory Monitoraggio Immunologico Terapie Cellulari (MITiCi), Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Eliana Ruggiero
- Experimental Hematology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Francesco Manfredi
- Experimental Hematology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Aurora Merolla
- Vita-Salute San Raffaele University, Milan, Italy
- Aurora Merolla
- Internal Medicine Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Elisa Cantarelli
- 1Biological Resource Center Centro Risorse Biologiche-Ospedale San Raffaele (CRB-OSR), Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Cristina Tresoldi
- 1Biological Resource Center Centro Risorse Biologiche-Ospedale San Raffaele (CRB-OSR), Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Claudia Pastori
- Immunobiology of Human Immunodeficiency Virus (HIV) Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Roberta Caccia
- 2Neurovirology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Francesca Sironi
- Viral Evolution and Transmission Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Ilaria Marzinotto
- 3Diabetes Research Institute, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ospedale San Raffaele, Milan, Italy
- Fabio Saliu
- Emerging Bacterial Pathogens Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Silvia Ghezzi
- 4Viral Pathogenesis and Biosafety Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Vito Lampasona
- 3Diabetes Research Institute, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) Ospedale San Raffaele, Milan, Italy
- Elisa Vicenzi
- 4Viral Pathogenesis and Biosafety Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Paola Cinque
- 2Neurovirology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Angelo Andrea Manfredi
- Autoimmunity and Vascular Inflammation Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Gabriella Scarlatti
- Viral Evolution and Transmission Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Paolo Dellabona
- Experimental Immunology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Lucia Lopalco
- Immunobiology of Human Immunodeficiency Virus (HIV) Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Clelia Di Serio
- 0University Centre for Statistics in the Biomedical Sciences (CUSSB), Vita-Salute San Raffaele University, Milan, Italy
- Mauro Malnati
- Viral Evolution and Transmission Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Fabio Ciceri
- Vita-Salute San Raffaele University, Milan, Italy
- Fabio Ciceri
- 5Hematology and Bone Marrow Transplant Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Patrizia Rovere-Querini
- Vita-Salute San Raffaele University, Milan, Italy
- Patrizia Rovere-Querini
- Internal Medicine Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Chiara Bonini
- Experimental Hematology Unit, Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Chiara Bonini
- Cell Therapy Immunomonitoring Laboratory Monitoraggio Immunologico Terapie Cellulari (MITiCi), Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS) San Raffaele Scientific Institute, Milan, Italy
- Chiara Bonini
- Vita-Salute San Raffaele University, Milan, Italy
- DOI
- https://doi.org/10.3389/fimmu.2024.1381091
- Journal volume & issue
-
Vol. 15
Abstract
IntroductionSARS-CoV-2 pandemic still poses a significant burden on global health and economy, especially for symptoms persisting beyond the acute disease. COVID-19 manifests with various degrees of severity and the identification of early biomarkers capable of stratifying patient based on risk of progression could allow tailored treatments.MethodsWe longitudinally analyzed 67 patients, classified according to a WHO ordinal scale as having Mild, Moderate, or Severe COVID-19. Peripheral blood samples were prospectively collected at hospital admission and during a 6-month follow-up after discharge. Several subsets and markers of the innate and adaptive immunity were monitored as putative factors associated with COVID-19 symptoms.ResultsMore than 50 immunological parameters were associated with disease severity. A decision tree including the main clinical, laboratory, and biological variables at admission identified low NK-cell precursors and CD14+CD91+ monocytes, and high CD8+ Effector Memory T cell frequencies as the most robust immunological correlates of COVID-19 severity and reduced survival. Moreover, low regulatory B-cell frequency at one month was associated with the susceptibility to develop long COVID at six months, likely due to their immunomodulatory ability.DiscussionThese results highlight the profound perturbation of the immune response during COVID-19. The evaluation of specific innate and adaptive immune-cell subsets allows to distinguish between different acute and persistent COVID-19 symptoms.
Keywords
- COVID-19 severity
- COVID-19 patients’ survival
- SARS-CoV-2 innate immunity
- SARS-CoV-2 adaptive immunity
- long COVID