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PLACENTAL TISSUE DESTRUCTION AND INSUFFICIENCY FROM COVID-19 CAUSES STILLBIRTH AND NEONATAL DEATH FROM HYPOXIC-ISCHEMIC INJURY: A STUDY OF 68 CASES WITH SARS-COV-2 PLACENTITIS FROM 12 COUNTRIES
Author
Schwartz, David A.
Avvad-Portari, Elyzabeth
Babál, Pavel
Baldewijns, Marcella
Blomberg, Marie
Bouachba, Amine
Camacho, Jessica
Collardeau-Frachon, Sophie
Colson, Arthur
Dehaene, Isabelle
Ferreres, Joan Carles
Fitzgerald, Brendan
Garrido-Pontnou, Marta
Gergis, Hazem
Hargitai, Beata
Helguera-Repetto, A. Cecilia
Holmström, Sandra
Irles, Claudine Liliane
Leijonhfvud, Åsa
Libbrecht, Sasha
Marton, Tamás
McEntagart, Noel
Molina, James T.
Morotti, Raffaella
Nadal, Alfons
Navarro, Alexandra
Nelander, Maria
Oviedo, Angelica
Otani, Andre Ricardo Oyamada
Papadogiannakis, Nikos
Petersen, Astrid C.
Roberts, Drucilla J.
Saad, Ali G.
Sand, Anna
Schoenmakers, Sam
Sehn, Jennifer K.
Simpson, Preston R.
Thomas, Kristen
Valdespino-Vázquez, M. Yolotzin
Van Der Meeren, Lotte E.
Van Dorpe, Jo
Verdijk, Robert M.
Watkins, Jaclyn C.
Zaigham, Mehreen
Avvad-Portari, Elyzabeth
Babál, Pavel
Baldewijns, Marcella
Blomberg, Marie
Bouachba, Amine
Camacho, Jessica
Collardeau-Frachon, Sophie
Colson, Arthur
Dehaene, Isabelle
Ferreres, Joan Carles
Fitzgerald, Brendan
Garrido-Pontnou, Marta
Gergis, Hazem
Hargitai, Beata
Helguera-Repetto, A. Cecilia
Holmström, Sandra
Irles, Claudine Liliane
Leijonhfvud, Åsa
Libbrecht, Sasha
Marton, Tamás
McEntagart, Noel
Molina, James T.
Morotti, Raffaella
Nadal, Alfons
Navarro, Alexandra
Nelander, Maria
Oviedo, Angelica
Otani, Andre Ricardo Oyamada
Papadogiannakis, Nikos
Petersen, Astrid C.
Roberts, Drucilla J.
Saad, Ali G.
Sand, Anna
Schoenmakers, Sam
Sehn, Jennifer K.
Simpson, Preston R.
Thomas, Kristen
Valdespino-Vázquez, M. Yolotzin
Van Der Meeren, Lotte E.
Van Dorpe, Jo
Verdijk, Robert M.
Watkins, Jaclyn C.
Zaigham, Mehreen
Affilliation
Sem afiliação.
Fundação Oswaldo Cruz. Instituto Nacional de Saúde da Mulher, da Criança e do Adolescente Fernandes Figueira. Departamento de Patologia. Rio de Janeiro, RJ, Brasil.
Comenius University. Faculty of Medicine. Department of Pathology. Bratislava, Slovakia.
University Hospitals Leuven. Department of Pathology. Leuven, Belgium.
Linköping University. Department of Obstetrics and Gynecology. Linköping, Sweden / Linköping University. Department of Biomedical and Clinical Sciences. Linköping, Sweden.
Hospices Civils de Lyon. Institut de Pathologie Multisite. Lyon, France / SOFFOET–Société Française de Fœtopathologie, Paris, France.
Hospital Universitari Vall d'Hebron. Pathology Department. Barcelona, Spain.
SOFFOET–Société Française de Fœtopathologie, Paris, France / Université Claude Bernard Lyon 1. Hospices Civils de Lyon. Hopital Femme-Mère Enfant. Department of Pathology. Bron, France.
Université Catholique de Louvain. Institute of Experimental and Clinical Research. Department of Obstetrics. Brussels, Belgium.
Ghent University Hospital. Department of Obstetrics and Gynaecology. Ghent, Belgium.
Institut d'Investigació i Innovació Parc Taulí I3PT. Parc Taulí Hospital Universitari. Pathology Department. Barcelona, Spain / Universitat Autònoma de Barcelona. School of Medicine. Department of Morphological Sciences. Sabadell, Spain.
Cork University Hospital. Department of Pathology. Wilton, Cork, Republic of Ireland.
Hospital Universitari Vall d'Hebron. Pathology Department. Barcelona, Spain / Universitat Autònoma de Barcelona. School of Medicine. Department of Morphological Sciences. Barcelona, Spain.
Women's Hospital. Doncaster and Bassetlaw NHS Teaching Hospitals. Department of Obstetrics and Gynaecology. Doncaster, United Kingdom.
NHS Foundation Trust. Birmingham Women's and Children's Hospital. Department of Cellular Pathology. Division of Perinatal Pathology. Birmingham, United Kingdom.
National Institute of Perinatology. Department of Immunobiochemistry. Mexico City, Mexico.
Halland Hospital. Department of Obstetrics and Gynaecology. Varberg, Sweden.
National Institute of Perinatology “Isidro Espinosa de los Reyes”. Department of Physiology and Cellular Development. Mexico City, Mexico.
Helsingborg Hospital. Department of Obstetrics and Gynaecology. Helsingborg, Sweden / Lund University. Department of Clinical Science Helsingborg. Lund, Sweden.
Antwerp University Hospital. Department of Pathological Anatomy. Edegem, Belgium.
Birmingham Women's Hospital. Cellular Pathology Department. Birmingham, United Kingdom.
Rotunda Hospital. Histopathology. Dublin, Republic of Ireland.
Sem afiliação.
Yale University School of Medicine. Autopsy Service. Department of Pathology and Pediatrics. New Haven, Connecticut.
Hospital Clínic. Pathology Department. Barcelona, Spain / Universitat de Barcelona. School of Medicine. Department of Basic Clinical Practice. Barcelona, Spain / August Pi i Sunyer Biomedical Research Institute. Barcelona, Spain.
Hospital Universitari Vall d'Hebron. Pathology Department. Barcelona, Spain.
Uppsala University. Department of Women's and Children's Health. Uppsala, Sweden.
Burrell College of Osteopathic Medicine. Department of Pathology and Laboratory Medicine. Las Cruces, New Mexico.
Laboratório Ferdinando Costa. São Paulo, SP, Brasil.
Karolinska University Hospital. Division of Pathology. Department of Laboratory Medicine. Stockholm, Sweden / Karolinska University Hospital. Departments of Pathology. Stockholm, Sweden.
Aalborg University Hospital. Department of Pathology. Aalborg, Denmark.
Harvard Medical School. Massachusetts General Hospital. Department of Pathology. Boston, Massachusetts.
University of Miami Miller School of Medicine/Jackson Health System/Holtz Children's Hospital. Department of Pathology. Pediatric Pathology and Neuropathology. Miami, Florida.
Karolinska Institute. Department of Women's and Children's Health. Stockholm, Sweden / Karolinska University Hospital. Department of Obstetrics and Gynaecology. Solna, Stockholm, Sweden.
University Medical Center Rotterdam. Department of Obstetrics and Gynaecology. Rotterdam, the Netherlands.
St. Louis University School of Medicine. Department of Pathology. St Louis, Missouri.
CHRISTUS Hospital St Elizabeth. Department of Pathology. Beaumont, Texas.
New York University School of Medicine. NYU Langone Health–Main Campus & Bellevue Hospital Center. Department of Pathology. New York, USA.
National Institute of Perinatology. Department of Anatomical Pathology. Mexico City, Mexico.
Leiden University Medical Center. Department of Pathology. Leiden, the Netherlands / University Medical Center Utrecht. Department of Pathology. Utrecht, the Netherlands.
Ghent University Hospital. Department of Pathology. Ghent, Belgium.
University Medical Center Rotterdam. Department of Obstetrics and Gynaecology. Rotterdam, the Netherlands.
Harvard Medical School. Massachusetts General Hospital. Department of Pathology. Boston, Massachusetts.
Lund University. Institution of Clinical Sciences Lund. Obstetrics & Gynecology. Lund, Sweden / Skåne University Hospital. Department of Obstetrics and Gynecology. Malmö and Lund, Sweden.
Fundação Oswaldo Cruz. Instituto Nacional de Saúde da Mulher, da Criança e do Adolescente Fernandes Figueira. Departamento de Patologia. Rio de Janeiro, RJ, Brasil.
Comenius University. Faculty of Medicine. Department of Pathology. Bratislava, Slovakia.
University Hospitals Leuven. Department of Pathology. Leuven, Belgium.
Linköping University. Department of Obstetrics and Gynecology. Linköping, Sweden / Linköping University. Department of Biomedical and Clinical Sciences. Linköping, Sweden.
Hospices Civils de Lyon. Institut de Pathologie Multisite. Lyon, France / SOFFOET–Société Française de Fœtopathologie, Paris, France.
Hospital Universitari Vall d'Hebron. Pathology Department. Barcelona, Spain.
SOFFOET–Société Française de Fœtopathologie, Paris, France / Université Claude Bernard Lyon 1. Hospices Civils de Lyon. Hopital Femme-Mère Enfant. Department of Pathology. Bron, France.
Université Catholique de Louvain. Institute of Experimental and Clinical Research. Department of Obstetrics. Brussels, Belgium.
Ghent University Hospital. Department of Obstetrics and Gynaecology. Ghent, Belgium.
Institut d'Investigació i Innovació Parc Taulí I3PT. Parc Taulí Hospital Universitari. Pathology Department. Barcelona, Spain / Universitat Autònoma de Barcelona. School of Medicine. Department of Morphological Sciences. Sabadell, Spain.
Cork University Hospital. Department of Pathology. Wilton, Cork, Republic of Ireland.
Hospital Universitari Vall d'Hebron. Pathology Department. Barcelona, Spain / Universitat Autònoma de Barcelona. School of Medicine. Department of Morphological Sciences. Barcelona, Spain.
Women's Hospital. Doncaster and Bassetlaw NHS Teaching Hospitals. Department of Obstetrics and Gynaecology. Doncaster, United Kingdom.
NHS Foundation Trust. Birmingham Women's and Children's Hospital. Department of Cellular Pathology. Division of Perinatal Pathology. Birmingham, United Kingdom.
National Institute of Perinatology. Department of Immunobiochemistry. Mexico City, Mexico.
Halland Hospital. Department of Obstetrics and Gynaecology. Varberg, Sweden.
National Institute of Perinatology “Isidro Espinosa de los Reyes”. Department of Physiology and Cellular Development. Mexico City, Mexico.
Helsingborg Hospital. Department of Obstetrics and Gynaecology. Helsingborg, Sweden / Lund University. Department of Clinical Science Helsingborg. Lund, Sweden.
Antwerp University Hospital. Department of Pathological Anatomy. Edegem, Belgium.
Birmingham Women's Hospital. Cellular Pathology Department. Birmingham, United Kingdom.
Rotunda Hospital. Histopathology. Dublin, Republic of Ireland.
Sem afiliação.
Yale University School of Medicine. Autopsy Service. Department of Pathology and Pediatrics. New Haven, Connecticut.
Hospital Clínic. Pathology Department. Barcelona, Spain / Universitat de Barcelona. School of Medicine. Department of Basic Clinical Practice. Barcelona, Spain / August Pi i Sunyer Biomedical Research Institute. Barcelona, Spain.
Hospital Universitari Vall d'Hebron. Pathology Department. Barcelona, Spain.
Uppsala University. Department of Women's and Children's Health. Uppsala, Sweden.
Burrell College of Osteopathic Medicine. Department of Pathology and Laboratory Medicine. Las Cruces, New Mexico.
Laboratório Ferdinando Costa. São Paulo, SP, Brasil.
Karolinska University Hospital. Division of Pathology. Department of Laboratory Medicine. Stockholm, Sweden / Karolinska University Hospital. Departments of Pathology. Stockholm, Sweden.
Aalborg University Hospital. Department of Pathology. Aalborg, Denmark.
Harvard Medical School. Massachusetts General Hospital. Department of Pathology. Boston, Massachusetts.
University of Miami Miller School of Medicine/Jackson Health System/Holtz Children's Hospital. Department of Pathology. Pediatric Pathology and Neuropathology. Miami, Florida.
Karolinska Institute. Department of Women's and Children's Health. Stockholm, Sweden / Karolinska University Hospital. Department of Obstetrics and Gynaecology. Solna, Stockholm, Sweden.
University Medical Center Rotterdam. Department of Obstetrics and Gynaecology. Rotterdam, the Netherlands.
St. Louis University School of Medicine. Department of Pathology. St Louis, Missouri.
CHRISTUS Hospital St Elizabeth. Department of Pathology. Beaumont, Texas.
New York University School of Medicine. NYU Langone Health–Main Campus & Bellevue Hospital Center. Department of Pathology. New York, USA.
National Institute of Perinatology. Department of Anatomical Pathology. Mexico City, Mexico.
Leiden University Medical Center. Department of Pathology. Leiden, the Netherlands / University Medical Center Utrecht. Department of Pathology. Utrecht, the Netherlands.
Ghent University Hospital. Department of Pathology. Ghent, Belgium.
University Medical Center Rotterdam. Department of Obstetrics and Gynaecology. Rotterdam, the Netherlands.
Harvard Medical School. Massachusetts General Hospital. Department of Pathology. Boston, Massachusetts.
Lund University. Institution of Clinical Sciences Lund. Obstetrics & Gynecology. Lund, Sweden / Skåne University Hospital. Department of Obstetrics and Gynecology. Malmö and Lund, Sweden.
Abstract
Context.—Perinatal death is an increasingly important problem as the coronavirus disease 2019 (COVID-19) pandemic continues, but the mechanism of death has been unclear. Objective.—To evaluate the role of the placenta in causing stillbirth and neonatal death following maternal infection with COVID-19 and confirmed placental positivity for severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Design.—Case-based retrospective clinicopathologic analysis by a multinational group of 44 perinatal specialists from 12 countries of placental and autopsy pathology findings from 64 stillborns and 4 neonatal deaths having placentas testing positive for SARS-CoV-2 following delivery to mothers with COVID-19. Results.—Of the 3 findings constituting SARS-CoV-2 placentitis, all 68 placentas had increased fibrin deposition and villous trophoblast necrosis and 66 had chronic histiocytic intervillositis. Sixty-three placentas had massive perivillous fibrin deposition. Severe destructive placental disease from SARS-CoV-2 placentitis averaged 77.7% tissue involvement. Other findings included multiple intervillous thrombi (37%; 25 of 68) and chronic villitis (32%; 22 of 68). The majority (19; 63%) of the 30 autopsies revealed no significant fetal abnormalities except for intrauterine hypoxia and asphyxia. Among all 68 cases, SARS-CoV-2 was detected from a body specimen in 16 of 28 cases tested, most frequently from nasopharyngeal swabs. Four autopsied stillborns had SARS-CoV-2 identified in internal organs. Conclusions.—The pathology abnormalities composing SARS-CoV-2 placentitis cause widespread and severe placental destruction resulting in placental malperfusion and insufficiency. In these cases, intrauterine and perinatal death likely results directly from placental insufficiency and fetal hypoxic-ischemic injury. There was no evidence that SARS-CoV-2 involvement of the fetus had a role in causing these deaths.
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