Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-18T02:18:07.930Z Has data issue: false hasContentIssue false

Ultracellular Imaging of Bronchoalveolar Lavage from Young COVID-19 Patients with Comorbidities Showed Greater SARS-COV-2 Infection but Lesser Ultrastructural Damage Than the Older Patients

Published online by Cambridge University Press:  06 September 2022

Shikha Chaudhary
Affiliation:
Electron Microscope Facility, Department of Anatomy, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Preeti Rai
Affiliation:
Electron Microscope Facility, Department of Anatomy, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Arti Joshi
Affiliation:
Electron Microscope Facility, Department of Anatomy, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Pooja Yadav
Affiliation:
Department of Pathology, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Kishore Sesham
Affiliation:
Electron Microscope Facility, Department of Anatomy, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Shailendra Kumar
Affiliation:
Department of Anaesthesiology, Pain Medicine and Critical Care, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Asit Ranjan Mridha
Affiliation:
Department of Pathology, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Upendra Baitha
Affiliation:
Department of Medicine, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Tapas Chandra Nag
Affiliation:
Electron Microscope Facility, Department of Anatomy, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Kapil Dev Soni
Affiliation:
Anaesthesia and Critical Care, JPN Apex Trauma Center, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Anjan Trikha
Affiliation:
Department of Anaesthesiology, Pain Medicine and Critical Care, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
Subhash Chandra Yadav*
Affiliation:
Electron Microscope Facility, Department of Anatomy, All India Institute of Medical Sciences, New Delhi, Delhi 110029, India
*
*Corresponding author: Subhash Chandra Yadav, E-mail: [email protected]
Get access

Abstract

In this study, we examined the cellular infectivity and ultrastructural changes due to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection in the various cells of bronchoalveolar fluid (BALF) from intubated patients of different age groups (≥60 years and <60 years) and with common comorbidities such as diabetes, liver and kidney diseases, and malignancies. BALF of 79 patients (38 cases >60 and 41 cases <60 years) were studied by light microscopy, immunofluorescence, scanning, and transmission electron microscopy to evaluate the ultrastructural changes in the ciliated epithelium, type II pneumocytes, macrophages, neutrophils, eosinophils, lymphocytes, and anucleated granulocytes. This study demonstrated relatively a greater infection and better preservation of subcellular structures in these cells from BALF of younger patients (<60 years compared with the older patients (≥60 years). The different cells of BALF from the patients without comorbidities showed higher viral load compared with the patients with comorbidities. Diabetic patients showed maximum ultrastructural damage in BALF cells in the comorbid group. This study highlights the comparative effect of SARS-CoV-2 infection on the different airway and inflammatory cells of BALF at the subcellular levels among older and younger patients and in patients with comorbid conditions.

Type
Biological Applications
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Agusti, A & Hogg, JC (2019). Update on the pathogenesis of chronic obstructive pulmonary disease. N Engl J Med 381(13), 12481256.CrossRefGoogle ScholarPubMed
Ahn, JH, Kim, J, Hong, SP, Choi, SY, Yang, MJ, Ju, YS, Kim, YT, Kim, HM, Rahman, MDT, Chung, MK, Hong, SD, Bae, H, Lee, CS & Koh, GY (2021). Nasal ciliated cells are primary targets for SARS-CoV-2 replication in the early stage of COVID-19. J Clin Invest 131(13), e148517.CrossRefGoogle ScholarPubMed
Alsobaie, S (2021). Understanding the molecular biology of SARS-CoV-2 and the COVID-19 pandemic: A review. Infect Drug Resist 14, 22592268.CrossRefGoogle ScholarPubMed
Andersen, KG, Rambaut, A, Lipkin, WI, Holmes, EC & Garry, RF (2020). The proximal origin of SARS-CoV-2. Nat Med 26(4), 450452.CrossRefGoogle ScholarPubMed
Bajaj, V, Gadi, N, Spihlman, AP, Wu, SC, Choi, CH & Moulton, VR (2020). Aging, immunity, and COVID-19: How age influences the host immune response to coronavirus infections? Front Physiol 11, 571416.CrossRefGoogle ScholarPubMed
Brinkmann, V, Reichard, U, Goosmann, C, Fauler, B, Uhlemann, Y, Weiss, DS, Weinrauch, Y & Zychlinsky, A (2004). Neutrophil extracellular traps kill bacteria. Science 303(5663), 15321535.CrossRefGoogle ScholarPubMed
Bunyavanich, S, Do, A & Vicencio, A (2020). Nasal gene expression of angiotensin-converting enzyme 2 in children and adults. JAMA 323(23), 24272429.CrossRefGoogle ScholarPubMed
Burnham, EL, Janssen, WJ, Riches, DW, Moss, M & Downey, GP (2014). The fibroproliferative response in acute respiratory distress syndrome: Mechanisms and clinical significance. Eur Respir J 43(1), 276285.CrossRefGoogle ScholarPubMed
Chaudhary, S, Rai, P, Sesham, K, Kumar, S, Singh, P, Nag, TC, Chaudhuri, P, Trikha, A & Yadav, SC (2021). Microscopic imaging of bronchoalveolar fluids of COVID-19 positive intubated patients reveals the different level of SARS-CoV-2 infection on oral squamosal epithelial cells. Indian J Biochem Biophys 58(3), 196207.Google Scholar
Chen, J, Jiang, Q, Xia, X, Liu, K, Yu, Z, Tao, W, Gong, W & Han, JJ (2020a). Individual variation of the SARS-CoV-2 receptor ACE2 gene expression and regulation. Aging Cell 19(7), e13168.CrossRefGoogle Scholar
Chen, X, Tang, J, Shuai, W, Meng, J, Feng, J & Han, Z (2020b). Macrophage polarization and its role in the pathogenesis of acute lung injury/acute respiratory distress syndrome. Inflamm Res 69(9), 883895.CrossRefGoogle Scholar
Ciaglia, E, Vecchione, C & Puca, AA (2020). COVID-19 Infection and circulating ACE2 levels: Protective role in women and children. Front Pediatr 8, 206.CrossRefGoogle ScholarPubMed
Codo, AC, Davanzo, GG, Monteiro, LB, de Souza, GF, Muraro, SP, Virgilio-da-Silva, JV, Prodonoff, JS, Carregari, VC, de Biagi Junior, CAO, Crunfli, F, Jimenez Restrepo, JL, Vendramini, PH, Reis-de-Oliveira, G, Bispo Dos Santos, K, Toledo-Teixeira, DA, Parise, PL, Martini, MC, Marques, RE, Carmo, HR, Borin, A, Coimbra, LD, Boldrini, VO, Brunetti, NS, Vieira, AS, Mansour, E, Ulaf, RG, Bernardes, AF, Nunes, TA, Ribeiro, LC, Palma, AC, Agrela, MV, Moretti, ML, Sposito, AC, Pereira, FB, Velloso, LA, Vinolo, MAR, Damasio, A, Proenca-Modena, JL, Carvalho, RF, Mori, MA, Martins-de-Souza, D, Nakaya, HI, Farias, AS & Moraes-Vieira, PM (2020). Elevated glucose levels favor SARS-CoV-2 infection and monocyte response through a HIF-1alpha/glycolysis-dependent axis. Cell Metab 32(3), 437446.CrossRefGoogle ScholarPubMed
Craver, R, Huber, S, Sandomirsky, M, McKenna, D, Schieffelin, J & Finger, L (2020). Fatal eosinophilic myocarditis in a healthy 17-year-old male with severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2c). Fetal Pediatr Pathol 39(3), 263268.CrossRefGoogle Scholar
da Silva da Costa, FA, Soares, MR, Malagutti-Ferreira, MJ, da Silva, GR, Livero, F & Ribeiro-Paes, JT (2021). Three-dimensional cell cultures as a research platform in lung diseases and COVID-19. Tissue Eng Regen Med 18(5), 735745.CrossRefGoogle ScholarPubMed
Dias, FF, Zarantonello, VC, Parreira, GG, Chiarini-Garcia, H & Melo, RC (2014). The intriguing ultrastructure of lipid body organelles within activated macrophages. Microsc Microanal 20(3), 869878.CrossRefGoogle ScholarPubMed
Du, Y, Tu, L, Zhu, P, Mu, M, Wang, R, Yang, P, Wang, X, Hu, C, Ping, R, Hu, P, Li, T, Cao, F, Chang, C, Hu, Q, Jin, Y & Xu, G (2020). Clinical features of 85 fatal cases of COVID-19 from Wuhan. A retrospective observational study. Am J Respir Crit Care Med 201(11), 13721379.CrossRefGoogle ScholarPubMed
Elbadawi, M & Efferth, T (2020). Organoids of human airways to study infectivity and cytopathy of SARS-CoV-2. Lancet Respir Med 8(7), e55e56.CrossRefGoogle ScholarPubMed
Fisher, D & Heymann, D (2020). Q&A: The novel coronavirus outbreak causing COVID-19. BMC Med 18(1), 57.CrossRefGoogle ScholarPubMed
Gill, SE, Yamashita, CM & Veldhuizen, RA (2017). Lung remodeling associated with recovery from acute lung injury. Cell Tissue Res 367(3), 495509.CrossRefGoogle ScholarPubMed
Guan, WJ, Ni, ZY, Hu, Y, Liang, WH, Ou, CQ, He, JX, Liu, L, Shan, H, Lei, CL, Hui, DSC, Du, B, Li, LJ, Zeng, G, Yuen, KY, Chen, RC, Tang, CL, Wang, T, Chen, PY, Xiang, J, Li, SY, Wang, JL, Liang, ZJ, Peng, YX, Wei, L, Liu, Y, Hu, YH, Peng, P, Wang, JM, Liu, JY, Chen, Z, Li, G, Zheng, ZJ, Qiu, SQ, Luo, J, Ye, CJ, Zhu, SY, Zhong, NS & for the China Medical Treatment Expert Group for COVID-19 (2020). Clinical characteristics of coronavirus disease 2019 in China. N Engl J Med 382(18), 17081720.CrossRefGoogle ScholarPubMed
Hamada, N, Kuwano, K, Yamada, M, Hagimoto, N, Hiasa, K, Egashira, K, Nakashima, N, Maeyama, T, Yoshimi, M & Nakanishi, Y (2005). Anti-vascular endothelial growth factor gene therapy attenuates lung injury and fibrosis in mice. J Immunol 175(2), 12241231.CrossRefGoogle ScholarPubMed
Herold, S, Gabrielli, NM & Vadasz, I (2013). Novel concepts of acute lung injury and alveolar-capillary barrier dysfunction. Am J Physiol Lung Cell Mol Physiol 305(10), L665L681.CrossRefGoogle ScholarPubMed
Hou, YJ, Okuda, K, Edwards, CE, Martinez, DR, Asakura, T, Dinnon, KH 3rd, Kato, T, Lee, RE, Yount, BL, Mascenik, TM, Chen, G, Olivier, KN, Ghio, A, Tse, LV, Leist, SR, Gralinski, LE, Schafer, A, Dang, H, Gilmore, R, Nakano, S, Sun, L, Fulcher, ML, Livraghi-Butrico, A, Nicely, NI, Cameron, M, Cameron, C, Kelvin, DJ, de Silva, A, Margolis, DM, Markmann, A, Bartelt, L, Zumwalt, R, Martinez, FJ, Salvatore, SP, Borczuk, A, Tata, PR, Sontake, V, Kimple, A, Jaspers, I, O'Neal, WK, Randell, SH, Boucher, RC & Baric, RS (2020). SARS-CoV-2 reverse genetics reveals a variable infection gradient in the respiratory tract. Cell 182(2), 429446.e14CrossRefGoogle ScholarPubMed
Hu, B, Guo, H, Zhou, P & Shi, ZL (2021). Characteristics of SARS-CoV-2 and COVID-19. Nat Rev Microbiol 19(3), 141154.CrossRefGoogle ScholarPubMed
Huang, C, Wang, Y, Li, X, Ren, L, Zhao, J, Hu, Y, Zhang, L, Fan, G, Xu, J, Gu, X, Cheng, Z, Yu, T, Xia, J, Wei, Y, Wu, W, Xie, X, Yin, W, Li, H, Liu, M, Xiao, Y, Gao, H, Guo, L, Xie, J, Wang, G, Jiang, R, Gao, Z, Jin, Q, Wang, J & Cao, B (2020). Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395(10223), 497506.CrossRefGoogle ScholarPubMed
Huang, N, Perez, P, Kato, T, Mikami, Y, Okuda, K, Gilmore, RC, Conde, CD, Gasmi, B, Stein, S, Beach, M, Pelayo, E, Maldonado, JO, Lafont, BA, Jang, SI, Nasir, N, Padilla, RJ, Murrah, VA, Maile, R, Lovell, W, Wallet, SM, Bowman, NM, Meinig, SL, Wolfgang, MC, Choudhury, SN, Novotny, M, Aevermann, BD, Scheuermann, RH, Cannon, G, Anderson, CW, Lee, RE, Marchesan, JT, Bush, M, Freire, M, Kimple, AJ, Herr, DL, Rabin, J, Grazioli, A, Das, S, French, BN, Pranzatelli, T, Chiorini, JA, Kleiner, DE, Pittaluga, S, Hewitt, SM, Burbelo, PD, Chertow, D, Consortium, NC-A, Oral, HCA, Craniofacial Biological, N, Frank, K, Lee, J, Boucher, RC, Teichmann, SA, Warner, BM & Byrd, KM (2021). SARS-CoV-2 infection of the oral cavity and saliva. Nat Med 27(5), 892903.CrossRefGoogle ScholarPubMed
Johnston, LK, Rims, CR, Gill, SE, McGuire, JK & Manicone, AM (2012). Pulmonary macrophage subpopulations in the induction and resolution of acute lung injury. Am J Respir Cell Mol Biol 47(4), 417426.CrossRefGoogle ScholarPubMed
Kalligeros, M, Shehadeh, F, Mylona, EK, Benitez, G, Beckwith, CG, Chan, PA & Mylonakis, E (2020). Association of obesity with disease severity among patients with coronavirus disease 2019. Obesity (Silver Spring) 28(7), 12001204.CrossRefGoogle ScholarPubMed
Kim, DM, Kim, Y, Seo, JW, Lee, J, Park, U, Ha, NY, Koh, J, Park, H, Lee, JW, Ro, HJ, Yun, NR, Kim, DY, Yoon, SH, Na, YS, Moon, DS, Lim, SC, Kim, CM, Jeon, K, Kang, JG, Jang, NY, Jeong, H, Kim, J, Cheon, S, Sohn, KM, Moon, JY, Kym, S, Han, SR, Lee, MS, Kim, HJ, Park, WY, Choi, JY, Shin, HW, Kim, HY, Cho, CH, Jeon, YK, Kim, YS & Cho, NH (2021). Enhanced eosinophil-mediated inflammation associated with antibody and complement-dependent pneumonic insults in critical COVID-19. Cell Rep 37(1), 109798.CrossRefGoogle ScholarPubMed
Kosyreva, A, Dzhalilova, D, Lokhonina, A, Vishnyakova, P & Fatkhudinov, T (2021). The role of macrophages in the pathogenesis of SARS-CoV-2-associated acute respiratory distress syndrome. Front Immunol 12, 682871.CrossRefGoogle ScholarPubMed
Lai, CC, Shih, TP, Ko, WC, Tang, HJ & Hsueh, PR (2020). Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) and coronavirus disease-2019 (COVID-19): The epidemic and the challenges. Int J Antimicrob Agents 55(3), 105924.CrossRefGoogle ScholarPubMed
Lauer, SA, Grantz, KH, Bi, Q, Jones, FK, Zheng, Q, Meredith, HR, Azman, AS, Reich, NG & Lessler, J (2020). The incubation period of coronavirus disease 2019 (COVID-19) from publicly reported confirmed cases: Estimation and application. Ann Intern Med 172(9), 577582.CrossRefGoogle ScholarPubMed
Leis-Dosil, VM, Saez Vicente, A & Lorido-Cortes, MM (2020). Eosinophilic panniculitis associated with COVID-19. Actas Dermosifiliogr (Engl Ed) 111(9), 804805.CrossRefGoogle ScholarPubMed
Li, Q, Guan, X, Wu, P, Wang, X, Zhou, L, Tong, Y, Ren, R, Leung, KSM, Lau, EHY, Wong, JY, Xing, X, Xiang, N, Wu, Y, Li, C, Chen, Q, Li, D, Liu, T, Zhao, J, Liu, M, Tu, W, Chen, C, Jin, L, Yang, R, Wang, Q, Zhou, S, Wang, R, Liu, H, Luo, Y, Liu, Y, Shao, G, Li, H, Tao, Z, Yang, Y, Deng, Z, Liu, B, Ma, Z, Zhang, Y, Shi, G, Lam, TTY, Wu, JT, Gao, GF, Cowling, BJ, Yang, B, Leung, GM & Feng, Z (2020). Early transmission dynamics in Wuhan, China, of novel coronavirus-infected pneumonia. N Engl J Med 382(13), 11991207.CrossRefGoogle ScholarPubMed
Li, X & Ma, X (2020). Acute respiratory failure in COVID-19: Is it “typical” ARDS? Crit Care 24(1), 198.CrossRefGoogle ScholarPubMed
Lindsley, AW, Schwartz, JT & Rothenberg, ME (2020). Eosinophil responses during COVID-19 infections and coronavirus vaccination. J Allergy Clin Immunol 146(1), 17.CrossRefGoogle ScholarPubMed
Liu, J, Li, Y, Liu, Q, Yao, Q, Wang, X, Zhang, H, Chen, R, Ren, L, Min, J, Deng, F, Yan, B, Liu, L, Hu, Z, Wang, M & Zhou, Y (2021). SARS-CoV-2 cell tropism and multiorgan infection. Cell Discov 7(1), 17.CrossRefGoogle ScholarPubMed
Liu, Y, Beyer, A & Aebersold, R (2016). On the dependency of cellular protein levels on mRNA abundance. Cell 165(3), 535550.CrossRefGoogle ScholarPubMed
Lu, R, Zhao, X, Li, J, Niu, P, Yang, B, Wu, H, Wang, W, Song, H, Huang, B, Zhu, N, Bi, Y, Ma, X, Zhan, F, Wang, L, Hu, T, Zhou, H, Hu, Z, Zhou, W, Zhao, L, Chen, J, Meng, Y, Wang, J, Lin, Y, Yuan, J, Xie, Z, Ma, J, Liu, WJ, Wang, D, Xu, W, Holmes, EC, Gao, GF, Wu, G, Chen, W, Shi, W & Tan, W (2020). Genomic characterisation and epidemiology of 2019 novel coronavirus: Implications for virus origins and receptor binding. Lancet 395(10224), 565574.CrossRefGoogle ScholarPubMed
Magro, C, Mulvey, JJ, Berlin, D, Nuovo, G, Salvatore, S, Harp, J, Baxter-Stoltzfus, A & Laurence, J (2020). Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: A report of five cases. Transl Res 220, 113.CrossRefGoogle ScholarPubMed
Martines, RB, Ritter, JM, Matkovic, E, Gary, J, Bollweg, BC, Bullock, H, Goldsmith, CS, Silva-Flannery, L, Seixas, JN, Reagan-Steiner, S, Uyeki, T, Denison, A, Bhatnagar, J, Shieh, WJ, Zaki, SR & Group, C-PW (2020). Pathology and pathogenesis of SARS-CoV-2 associated with fatal coronavirus disease, United States. Emerg Infect Dis 26(9), 20052015.CrossRefGoogle ScholarPubMed
Mason, C, Dooley, N & Griffiths, M (2016). Acute respiratory distress syndrome. Clin Med (Lond) 16(Suppl 6), s66s70.CrossRefGoogle ScholarPubMed
Mason, RJ (2020). Thoughts on the alveolar phase of COVID-19. Am J Physiol Lung Cell Mol Physiol 319(1), L115L120.CrossRefGoogle ScholarPubMed
Matuschak, GM & Lechner, AJ (2010). Acute lung injury and the acute respiratory distress syndrome: Pathophysiology and treatment. Mo Med 107(4), 252258.Google ScholarPubMed
Mehta, P, McAuley, DF, Brown, M, Sanchez, E, Tattersall, RS, Manson, JJ & on behalf of the HLH Across Speciality Collaboration, UK (2020). COVID-19: Consider cytokine storm syndromes and immunosuppression. Lancet 395(10229), 10331034.CrossRefGoogle ScholarPubMed
Middleton, EA, He, XY, Denorme, F, Campbell, RA, Ng, D, Salvatore, SP, Mostyka, M, Baxter-Stoltzfus, A, Borczuk, AC, Loda, M, Cody, MJ, Manne, BK, Portier, I, Harris, ES, Petrey, AC, Beswick, EJ, Caulin, AF, Iovino, A, Abegglen, LM, Weyrich, AS, Rondina, MT, Egeblad, M, Schiffman, JD & Yost, CC (2020). Neutrophil extracellular traps contribute to immunothrombosis in COVID-19 acute respiratory distress syndrome. Blood 136(10), 11691179.CrossRefGoogle ScholarPubMed
Otsuka, R & Seino, KI (2020). Macrophage activation syndrome and COVID-19. Inflamm Regen 40, 19.CrossRefGoogle ScholarPubMed
Pan, Y, Guan, H, Zhou, S, Wang, Y, Li, Q, Zhu, T, Hu, Q & Xia, L (2020). Initial CT findings and temporal changes in patients with the novel coronavirus pneumonia (2019-nCoV): A study of 63 patients in Wuhan, China. Eur Radiol 30(6), 33063309.CrossRefGoogle ScholarPubMed
Pelosi, P & Rocco, PR (2008). Effects of mechanical ventilation on the extracellular matrix. Intensive Care Med 34(4), 631639.CrossRefGoogle ScholarPubMed
Perico, L, Benigni, A & Remuzzi, G (2020). Should COVID-19 concern nephrologists? Why and to what extent? The emerging impasse of angiotensin blockade. Nephron 144(5), 213221.CrossRefGoogle ScholarPubMed
Perlman, S & Dandekar, AA (2005). Immunopathogenesis of coronavirus infections: Implications for SARS. Nat Rev Immunol 5(12), 917927.Google ScholarPubMed
Ponomareva, AA, Nevzorova, TA, Mordakhanova, ER, Andrianova, IA, Rauova, L, Litvinov, RI & Weisel, JW (2017). Intracellular origin and ultrastructure of platelet-derived microparticles. J Thromb Haemost 15(8), 16551667.CrossRefGoogle ScholarPubMed
Richardson, S, Hirsch, JS, Narasimhan, M, Crawford, JM, McGinn, T, Davidson, KW, the Northwell C-RC, Barnaby, DP, Becker, LB, Chelico, JD, Cohen, SL, Cookingham, J, Coppa, K, Diefenbach, MA, Dominello, AJ, Duer-Hefele, J, Falzon, L, Gitlin, J, Hajizadeh, N, Harvin, TG, Hirschwerk, DA, Kim, EJ, Kozel, ZM, Marrast, LM, Mogavero, JN, Osorio, GA, Qiu, M & Zanos, TP (2020). Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized With COVID-19 in the New York city area. JAMA 323(20), 20522059.CrossRefGoogle ScholarPubMed
Rothan, HA & Byrareddy, SN (2020). The epidemiology and pathogenesis of coronavirus disease (COVID-19) outbreak. J Autoimmun 109, 102433.CrossRefGoogle ScholarPubMed
Rydell-Tormanen, K, Uller, L & Erjefalt, JS (2006). Direct evidence of secondary necrosis of neutrophils during intense lung inflammation. Eur Respir J 28(2), 268274.CrossRefGoogle ScholarPubMed
Salahudeen, AA, Choi, SS, Rustagi, A, Zhu, J, van Unen, V, de la, OS, Flynn, RA, Margalef-Catala, M, Santos, AJM, Ju, J, Batish, A, Usui, T, Zheng, GXY, Edwards, CE, Wagar, LE, Luca, V, Anchang, B, Nagendran, M, Nguyen, K, Hart, DJ, Terry, JM, Belgrader, P, Ziraldo, SB, Mikkelsen, TS, Harbury, PB, Glenn, JS, Garcia, KC, Davis, MM, Baric, RS, Sabatti, C, Amieva, MR, Blish, CA, Desai, TJ & Kuo, CJ (2020). Progenitor identification and SARS-CoV-2 infection in human distal lung organoids. Nature 588(7839), 670675.CrossRefGoogle ScholarPubMed
Sanyaolu, A, Okorie, C, Marinkovic, A, Patidar, R, Younis, K, Desai, P, Hosein, Z, Padda, I, Mangat, J & Altaf, M (2020). Comorbidity and its impact on patients with COVID-19. SN Compr Clin Med 2(8), 10691076.CrossRefGoogle ScholarPubMed
Shi, Q, Wang, Z, Liu, J, Wang, X, Zhou, Q, Li, Q, Yu, Y, Luo, Z, Liu, E, Chen, Y & COVID-19 Evidence and Recommendations Working Group (2021). Risk factors for poor prognosis in children and adolescents with COVID-19: A systematic review and meta-analysis. EClinicalMedicine 41, 101155.CrossRefGoogle ScholarPubMed
Silvestre-Roig, C, Fridlender, ZG, Glogauer, M & Scapini, P (2019). Neutrophil diversity in health and disease. Trends Immunol 40(7), 565583.CrossRefGoogle ScholarPubMed
Singh, M, Bansal, V & Feschotte, C (2020). A single-cell RNA expression map of human coronavirus entry factors. Cell Rep 32(12), 108175.CrossRefGoogle ScholarPubMed
Skendros, P, Mitsios, A, Chrysanthopoulou, A, Mastellos, DC, Metallidis, S, Rafailidis, P, Ntinopoulou, M, Sertaridou, E, Tsironidou, V, Tsigalou, C, Tektonidou, M, Konstantinidis, T, Papagoras, C, Mitroulis, I, Germanidis, G, Lambris, JD & Ritis, K (2020). Complement and tissue factor-enriched neutrophil extracellular traps are key drivers in COVID-19 immunothrombosis. J Clin Invest 130(11), 61516157.CrossRefGoogle ScholarPubMed
Spinelli, E, Mauri, T, Beitler, JR, Pesenti, A & Brodie, D (2020). Respiratory drive in the acute respiratory distress syndrome: Pathophysiology, monitoring, and therapeutic interventions. Intensive Care Med 46(4), 606618.CrossRefGoogle ScholarPubMed
Sungnak, W, Huang, N, Becavin, C, Berg, M, Queen, R, Litvinukova, M, Talavera-Lopez, C, Maatz, H, Reichart, D, Sampaziotis, F, Worlock, KB, Yoshida, M, Barnes, JL & Network, HCALB (2020). SARS-CoV-2 entry factors are highly expressed in nasal epithelial cells together with innate immune genes. Nat Med 26(5), 681687.CrossRefGoogle ScholarPubMed
Sur Chowdhury, C, Giaglis, S, Walker, UA, Buser, A, Hahn, S & Hasler, P (2014). Enhanced neutrophil extracellular trap generation in rheumatoid arthritis: Analysis of underlying signal transduction pathways and potential diagnostic utility. Arthritis Res Ther 16(3), R122.CrossRefGoogle ScholarPubMed
Tasaka, S, Amaya, F, Hashimoto, S & Ishizaka, A (2008). Roles of oxidants and redox signaling in the pathogenesis of acute respiratory distress syndrome. Antioxid Redox Signal 10(4), 739753.CrossRefGoogle ScholarPubMed
Tian, S, Xiong, Y, Liu, H, Niu, L, Guo, J, Liao, M & Xiao, SY (2020). Pathological study of the 2019 novel coronavirus disease (COVID-19) through postmortem core biopsies. Mod Pathol 33(6), 10071014.CrossRefGoogle ScholarPubMed
Tremblay, LN, Miatto, D, Hamid, Q, Govindarajan, A & Slutsky, AS (2002). Injurious ventilation induces widespread pulmonary epithelial expression of tumor necrosis factor-alpha and interleukin-6 messenger RNA. Crit Care Med 30(8), 16931700.CrossRefGoogle ScholarPubMed
Tyrrell, C, McKechnie, SR, Beers, MF, Mitchell, TJ & McElroy, MC (2012). Differential alveolar epithelial injury and protein expression in pneumococcal pneumonia. Exp Lung Res 38(5), 266276.CrossRefGoogle ScholarPubMed
Veras, FP, Pontelli, MC, Silva, CM, Toller-Kawahisa, JE, de Lima, M, Nascimento, DC, Schneider, AH, Caetite, D, Tavares, LA, Paiva, IM, Rosales, R, Colon, D, Martins, R, Castro, IA, Almeida, GM, Lopes, MIF, Benatti, MN, Bonjorno, LP, Giannini, MC, Luppino-Assad, R, Almeida, SL, Vilar, F, Santana, R, Bollela, VR, Auxiliadora-Martins, M, Borges, M, Miranda, CH, Pazin-Filho, A, da Silva, LLP, Cunha, LD, Zamboni, DS, Dal-Pizzol, F, Leiria, LO, Siyuan, L, Batah, S, Fabro, A, Mauad, T, Dolhnikoff, M, Duarte-Neto, A, Saldiva, P, Cunha, TM, Alves-Filho, JC, Arruda, E, Louzada-Junior, P, Oliveira, RD & Cunha, FQ (2020). SARS-CoV-2-triggered neutrophil extracellular traps mediate COVID-19 pathology. J Exp Med 217(12), e20201129.CrossRefGoogle ScholarPubMed
Verdecchia, P, Cavallini, C, Spanevello, A & Angeli, F (2020). The pivotal link between ACE2 deficiency and SARS-CoV-2 infection. Eur J Intern Med 76, 1420.CrossRefGoogle ScholarPubMed
V'Kovski, P, Kratzel, A, Steiner, S, Stalder, H & Thiel, V (2021). Coronavirus biology and replication: Implications for SARS-CoV-2. Nat Rev Microbiol 19(3), 155170.CrossRefGoogle ScholarPubMed
Wan, HC, Melo, RC, Jin, Z, Dvorak, AM & Weller, PF (2007). Roles and origins of leukocyte lipid bodies: Proteomic and ultrastructural studies. FASEB J 21(1), 167178.CrossRefGoogle ScholarPubMed
Wang, D, Hu, B, Hu, C, Zhu, F, Liu, X, Zhang, J, Wang, B, Xiang, H, Cheng, Z, Xiong, Y, Zhao, Y, Li, Y, Wang, X & Peng, Z (2020a). Clinical characteristics of 138 hospitalized patients With 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA 323(11), 10611069.CrossRefGoogle Scholar
Wang, S, Li, Z, Wang, X, Zhang, S, Gao, P & Shi, Z (2021). The role of pulmonary surfactants in the treatment of acute respiratory distress syndrome in COVID-19. Front Pharmacol 12, 698905.CrossRefGoogle ScholarPubMed
Wang, W, Tang, J & Wei, F (2020b). Updated understanding of the outbreak of 2019 novel coronavirus (2019-nCoV) in Wuhan, China. J Med Virol 92(4), 441447.CrossRefGoogle Scholar
Wang, WK, Chen, SY, Liu, IJ, Chen, YC, Chen, HL, Yang, CF, Chen, PJ, Yeh, SH, Kao, CL, Huang, LM, Hsueh, PR, Wang, JT, Sheng, WH, Fang, CT, Hung, CC, Hsieh, SM, Su, CP, Chiang, WC, Yang, JY, Lin, JH, Hsieh, SC, Hu, HP, Chiang, YP, Wang, JT, Yang, PC, Chang, SC & members of the SARS Research Group of the National Taiwan University, and National Taiwan University Hospital (2004). Detection of SARS-associated coronavirus in throat wash and saliva in early diagnosis. Emerg Infect Dis 10(7), 12131219.CrossRefGoogle ScholarPubMed
Wauters, E, Van Mol, P, Garg, AD, Jansen, S, Van Herck, Y, Vanderbeke, L, Bassez, A, Boeckx, B, Malengier-Devlies, B, Timmerman, A, Van Brussel, T, Van Buyten, T, Schepers, R, Heylen, E, Dauwe, D, Dooms, C, Gunst, J, Hermans, G, Meersseman, P, Testelmans, D, Yserbyt, J, Tejpar, S, De Wever, W, Matthys, P, CONTAGIOUS collaborators, Neyts J, Wauters J, Qian J & Lambrechts D (2021). Discriminating mild from critical COVID-19 by innate and adaptive immune single-cell profiling of bronchoalveolar lavages. Cell Res 31(3), 272290.CrossRefGoogle ScholarPubMed
Weller, PF & Spencer, LA (2017). Functions of tissue-resident eosinophils. Nat Rev Immunol 17(12), 746760.CrossRefGoogle ScholarPubMed
Wheeler, AP & Bernard, GR (2007). Acute lung injury and the acute respiratory distress syndrome: A clinical review. Lancet 369(9572), 15531564.CrossRefGoogle ScholarPubMed
Williamson, EJ, Walker, AJ, Bhaskaran, K, Bacon, S, Bates, C, Morton, CE, Curtis, HJ, Mehrkar, A, Evans, D, Inglesby, P, Cockburn, J, McDonald, HI, MacKenna, B, Tomlinson, L, Douglas, IJ, Rentsch, CT, Mathur, R, Wong, AYS, Grieve, R, Harrison, D, Forbes, H, Schultze, A, Croker, R, Parry, J, Hester, F, Harper, S, Perera, R, Evans, SJW, Smeeth, L & Goldacre, B (2020). Factors associated with COVID-19-related death using OpenSAFELY. Nature 584(7821), 430436.CrossRefGoogle ScholarPubMed
Wong, SL, Demers, M, Martinod, K, Gallant, M, Wang, Y, Goldfine, AB, Kahn, CR & Wagner, DD (2015). Diabetes primes neutrophils to undergo NETosis, which impairs wound healing. Nat Med 21(7), 815819.CrossRefGoogle ScholarPubMed
Wood, C, Kataria, V & Modrykamien, AM (2020). The acute respiratory distress syndrome. In Baylor University Medical Center Proceedings, Vol. 33, No. 3, pp. 357–365. Taylor & Francis.CrossRefGoogle Scholar
Wu, C, Chen, X, Cai, Y, Xia, J, Zhou, X, Xu, S, Huang, H, Zhang, L, Zhou, X, Du, C, Zhang, Y, Song, J, Wang, S, Chao, Y, Yang, Z, Xu, J, Zhou, X, Chen, D, Xiong, W, Xu, L, Zhou, F, Jiang, J, Bai, C, Zheng, J & Song, Y (2020). Risk factors associated with acute respiratory distress syndrome and death in patients with coronavirus disease 2019 pneumonia in Wuhan, China. JAMA Intern Med 180(7), 934943.CrossRefGoogle ScholarPubMed
Xu, Z, Shi, L, Wang, Y, Zhang, J, Huang, L, Zhang, C, Liu, S, Zhao, P, Liu, H, Zhu, L, Tai, Y, Bai, C, Gao, T, Song, J, Xia, P, Dong, J, Zhao, J & Wang, FS (2020). Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respir Med 8(4), 420422.CrossRefGoogle ScholarPubMed
Yanez, ND, Weiss, NS, Romand, JA & Treggiari, MM (2020). COVID-19 mortality risk for older men and women. BMC Public Health 20(1), 1742.CrossRefGoogle ScholarPubMed
Yang, MS, Oh, BK, Yang, D, Oh, EY, Kim, Y, Kang, KW, Lim, CW, Koh, GY, Lee, SM & Kim, B (2021). Ultra- and micro-structural changes of respiratory tracts in SARS-CoV-2 infected Syrian hamsters. Vet Res 52(1), 121.CrossRefGoogle ScholarPubMed
Yazdanpanah, F, Hamblin, MR & Rezaei, N (2020). The immune system and COVID-19: Friend or foe? Life Sci 256, 117900.CrossRefGoogle ScholarPubMed
Zamorano Cuervo, N & Grandvaux, N (2020). ACE2: Evidence of role as entry receptor for SARS-CoV-2 and implications in comorbidities. Elife 9, e61390.CrossRefGoogle ScholarPubMed
Zhang, Q, Xiang, R, Huo, S, Zhou, Y, Jiang, S, Wang, Q & Yu, F (2021). Molecular mechanism of interaction between SARS-CoV-2 and host cells and interventional therapy. Signal Transduct Target Ther 6(1), 233.CrossRefGoogle ScholarPubMed
Zhao, J, Zhou, H, Huang, W, Zhou, J, Qiu, M, Deng, Z, Chen, L, Weng, Y, Cai, L, Gu, Y, Zheng, Q, Chen, Q, Hou, X, Wang, L, Shen, L & Yang, Z (2020). Cell morphological analysis of SARS-CoV-2 infection by transmission electron microscopy. J Thorac Dis 12(8), 43684373.CrossRefGoogle ScholarPubMed
Zhou, F, Yu, T, Du, R, Fan, G, Liu, Y, Liu, Z, Xiang, J, Wang, Y, Song, B, Gu, X, Guan, L, Wei, Y, Li, H, Wu, X, Xu, J, Tu, S, Zhang, Y, Chen, H & Cao, B (2020). Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: A retrospective cohort study. Lancet 395(10229), 10541062.CrossRefGoogle ScholarPubMed
Supplementary material: File

Chaudhary et al. supplementary material

Chaudhary et al. supplementary material

Download Chaudhary et al. supplementary material(File)
File 7.8 MB