Sex differences in immune responses that underlie COVID-19 disease outcomes

Takehiro Takahashi, Mallory K. Ellingson, Patrick Wong, Benjamin Israelow, Carolina Lucas, Jon Klein, Julio Silva, Tianyang Mao, Ji Eun Oh, Maria Tokuyama, Peiwen Lu, Arvind Venkataraman, Annsea Park, Feimei Liu, Amit Meir, Jonathan Sun, Eric Y. Wang, Arnau Casanovas-Massana, Anne L. Wyllie, Chantal B. F. Vogels, Rebecca Earnest, Sarah Lapidus, Isabel M. Ott, Adam J. Moore, Albert Shaw, John B. Fournier, Camila D. Odio, Shelli Farhadian, Charles Cruz, Nathan D. Grubaugh, Wade L. Schulz, Aaron M. Ring, Albert I. Ko, Saad B. Omer and Akiko Iwasaki ()
Additional contact information
Takehiro Takahashi: Yale University School of Medicine
Mallory K. Ellingson: Yale School of Public Health
Patrick Wong: Yale University School of Medicine
Benjamin Israelow: Yale University School of Medicine
Carolina Lucas: Yale University School of Medicine
Jon Klein: Yale University School of Medicine
Julio Silva: Yale University School of Medicine
Tianyang Mao: Yale University School of Medicine
Ji Eun Oh: Yale University School of Medicine
Maria Tokuyama: Yale University School of Medicine
Peiwen Lu: Yale University School of Medicine
Arvind Venkataraman: Yale University School of Medicine
Annsea Park: Yale University School of Medicine
Feimei Liu: Yale University School of Medicine
Amit Meir: Yale University
Jonathan Sun: Yale University School of Medicine
Eric Y. Wang: Yale University School of Medicine
Arnau Casanovas-Massana: Yale School of Public Health
Anne L. Wyllie: Yale School of Public Health
Chantal B. F. Vogels: Yale School of Public Health
Rebecca Earnest: Yale School of Public Health
Sarah Lapidus: Yale School of Public Health
Isabel M. Ott: Yale School of Public Health
Adam J. Moore: Yale School of Public Health
Albert Shaw: Yale University School of Medicine
John B. Fournier: Yale University School of Medicine
Camila D. Odio: Yale University School of Medicine
Shelli Farhadian: Yale University School of Medicine
Charles Cruz: Yale University School of Medicine
Nathan D. Grubaugh: Yale School of Public Health
Wade L. Schulz: Yale University School of Medicine
Aaron M. Ring: Yale University School of Medicine
Albert I. Ko: Yale School of Public Health
Saad B. Omer: Yale School of Public Health
Akiko Iwasaki: Yale University School of Medicine

Nature, 2020, vol. 588, issue 7837, 315-320

Abstract: Abstract There is increasing evidence that coronavirus disease 2019 (COVID-19) produces more severe symptoms and higher mortality among men than among women1–5. However, whether immune responses against severe acute respiratory syndrome coronavirus (SARS-CoV-2) differ between sexes, and whether such differences correlate with the sex difference in the disease course of COVID-19, is currently unknown. Here we examined sex differences in viral loads, SARS-CoV-2-specific antibody titres, plasma cytokines and blood-cell phenotyping in patients with moderate COVID-19 who had not received immunomodulatory medications. Male patients had higher plasma levels of innate immune cytokines such as IL-8 and IL-18 along with more robust induction of non-classical monocytes. By contrast, female patients had more robust T cell activation than male patients during SARS-CoV-2 infection. Notably, we found that a poor T cell response negatively correlated with patients’ age and was associated with worse disease outcome in male patients, but not in female patients. By contrast, higher levels of innate immune cytokines were associated with worse disease progression in female patients, but not in male patients. These findings provide a possible explanation for the observed sex biases in COVID-19, and provide an important basis for the development of a sex-based approach to the treatment and care of male and female patients with COVID-19.

Date: 2020
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DOI: 10.1038/s41586-020-2700-3

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