Progress in research on osteoporosis secondary to SARS-CoV-2 infection

Jinlong Wang , Yibai Xiong , Zhiqi Song , Yanhong Li , Ling Zhang , Chuan Qin

Animal Models and Experimental Medicine ›› 2025, Vol. 8 ›› Issue (5) : 829 -841.

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Animal Models and Experimental Medicine ›› 2025, Vol. 8 ›› Issue (5) : 829 -841. DOI: 10.1002/ame2.12573
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Progress in research on osteoporosis secondary to SARS-CoV-2 infection

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Abstract

The World Health Organization has declared that COVID-19 no longer constitutes a “public health emergency of international concern,” yet the long-term impact of SARS-CoV-2 infection on bone health continues to pose new challenges for global public health. In recent years, numerous animal model and clinical studies have revealed that severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) infection can lead to secondary osteoporosis. The mechanisms involved are related to the virus's direct effects on bone tissue, dysregulation of the body's inflammatory response, hypoxia, noncoding RNA imbalance, and metabolic abnormalities. Although these studies have unveiled the connection between SARS-CoV-2 infection and osteoporosis, current research is not comprehensive and in depth. Future studies are needed to evaluate the long-term effects of SARS-CoV-2 on bone density and metabolism, elucidate the specific mechanisms of pathogenesis, and explore potential interventions. This review aims to collate existing research literature on SARS-CoV-2 infection-induced secondary osteoporosis, summarize the underlying mechanisms, and provide direction for future research.

Keywords

bone metabolism / COVID-19 / long COVID / osteoporosis / SARS-CoV-2

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Jinlong Wang, Yibai Xiong, Zhiqi Song, Yanhong Li, Ling Zhang, Chuan Qin. Progress in research on osteoporosis secondary to SARS-CoV-2 infection. Animal Models and Experimental Medicine, 2025, 8(5): 829-841 DOI:10.1002/ame2.12573

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References

[1]

World Health Organisation. Statement on the Fifteenth Meeting of the International Health Regulations (2005) Emergency Committee Regarding the Coronavirus Disease (COVID-19) Pandemic. World Health Organisation; 2005. https://www.who.int/news/item/05-05-2023-statement-on-the-fifteenth-meeting-of-the-international-health-regulations-(2005)-emergency-committee-regarding-the-coronavirus-disease-(covid-19)-pandemic

[2]

Zheng KI, Feng G, Liu WY, Targher G, Byrne CD, Zheng MH. Extrapulmonary complications of COVID-19: a multisystem disease? J Med Virol. 2021; 93: 323-335.

[3]

Schultze JL, Aschenbrenner AC. COVID-19 and the human innate immune system. Cell. 2021; 184: 1671-1692.

[4]

Kerschan-Schindl K, Dovjak P, Butylina M, et al. Moderate COVID-19 disease is associated with reduced bone turnover. J Bone Miner Res. 2023; 38: 943-950.

[5]

Xiong Y, Bao L, Ma Y, Zhang L, Qin C, Huang L. Wen-Yi and Chinese medicine: why we need to pay attention? Sci Bull (Beijing). 2024; 69: 1617-1622.

[6]

Ma Y, Lu D, Bao L, et al. SARS-CoV-2 infection aggravates chronic comorbidities of cardiovascular diseases and diabetes in mice. Anim Models and Exp Med. 2021; 4: 2-15.

[7]

Awosanya OD, Dalloul CE, Blosser RJ, et al. Osteoclast-mediated bone loss observed in a COVID-19 mouse model. Bone. 2022; 154: 116227.

[8]

Behera J, Ison J, Voor MJ, Tyagi SC, Tyagi N. Diabetic Covid-19 severity: impaired glucose tolerance and pathologic bone loss. Biochem Biophys Res Commun. 2022; 620: 180-187.

[9]

Haudenschild AK, Christiansen BA, Orr S, et al. Acute bone loss following SARS-CoV-2 infection in mice. J Orthop Res. 2023; 41: 1945-1952.

[10]

Qiao W, Lau HE, Xie H, et al. SARS-CoV-2 infection induces inflammatory bone loss in golden Syrian hamsters. Nat Commun. 2022; 13: 2539.

[11]

Berktaş BM, Gökçek A, Hoca NT, Koyuncu A. COVID-19 illness and treatment decrease bone mineral density of surviving hospitalized patients. Eur Rev Med Pharmacol Sci. 2022; 26: 3046-3056.

[12]

Elmedany SH, Badr OI, Abu-Zaid MH, Tabra SAA. Bone mineral density changes in osteoporotic and osteopenic patients after COVID-19 infection. Egypt Rheumatol Rehabil. 2022; 49: 64.

[13]

AL-Azzawi IS, Mohammed NS. The impact of angiotensin converting Enzyme-2 (ACE-2) on bone remodeling marker Osteoprotegerin (OPG) in post-COVID-19 Iraqi patients. Cureus. 2022; 14: e29926.

[14]

Queiroz-Junior CM, Santos ACPM, Gonçalves MR, et al. Acute coronavirus infection triggers a TNF-dependent osteoporotic phenotype in mice. Life Sci. 2023; 324: 121750.

[15]

Chan JF-W, Zhang AJ, Yuan S, et al. Simulation of the clinical and pathological manifestations of coronavirus disease 2019 (COVID-19) in a Golden Syrian hamster model: implications for disease pathogenesis and transmissibility. Clin Infect Dis. 2020; ciaa325: 2428-2446.

[16]

Qi F, Qin C. Characteristics of animal models for COVID-19. Anim Models and Exp Med. 2022; 5: 401-409.

[17]

Buccino F, Zagra L, Longo E, et al. Osteoporosis and Covid-19: detected similarities in bone lacunar-level alterations via combined AI and advanced synchrotron testing. Mater Des. 2023; 231: 112087.

[18]

Kottlors J, Große Hokamp N, Fervers P, et al. Early extrapulmonary prognostic features in chest computed tomography in COVID-19 pneumonia: bone mineral density is a relevant predictor for the clinical outcome - a multicenter feasibility study. Bone. 2021; 144: 115790.

[19]

Watanabe R, Shiraki M, Saito M, Okazaki R, Inoue D. Restrictive pulmonary dysfunction is associated with vertebral fractures and bone loss in elderly postmenopausal women. Osteoporos Int. 2018; 29: 625-633.

[20]

Kim B, Kim J, Jo YH, et al. Risk of pneumonia after vertebral compression fracture in women with low bone density: a population-based study. Spine. 2018; 43: E830-E835.

[21]

Di Filippo L. Radiological thoracic vertebral fractures are highly prevalent in COVID-19 and predict disease outcomes. J Clin Endocrinol Metab. 2021; 106: e602-e614.

[22]

Battisti S, Napoli N, Pedone C, et al. Vertebral fractures and mortality risk in hospitalised patients during the COVID-19 pandemic emergency. Endocrine. 2021; 74: 461-469.

[23]

Di Filippo L, Compagnone N, Frara S, et al. Vertebral fractures at hospitalization predict impaired respiratory function during follow-up of COVID-19 survivors. Endocrine. 2022; 77: 392-400.

[24]

Puig-Domingo M, Marazuela M, Giustina A. COVID-19 and endocrine diseases. A statement from the European society of endocrinology. Endocrine. 2020; 68: 2-5.

[25]

Marazuela M, Giustina A, Puig-Domingo M. Endocrine and metabolic aspects of the COVID-19 pandemic. Rev Endocr Metab Disord. 2020; 21: 495-507.

[26]

Giustina A. Hypovitaminosis D and the endocrine phenotype of COVID-19. Endocrine. 2021; 72: 1-11.

[27]

Giustina A, Marazuela M, Reincke M, Yildiz BO, Puig-Domingo M. One year of the pandemic-how European endocrinologists responded to the crisis: a statement from the European Society of Endocrinology. Eur J Endocrinol. 2021; 185: C1-C7.

[28]

Giustina A, Bilezikian JP. Revisiting the endocrine and metabolic manifestations of COVID-19 two years into the pandemic. Rev Endocr Metab Disord. 2022; 23: 133-136.

[29]

Tahtabasi M, Kilicaslan N, Akin Y, et al. The prognostic value of vertebral bone density on chest CT in hospitalized COVID-19 patients. J Clin Densitom. 2021; 24: 506-515.

[30]

Ferrari SL, Abrahamsen B, Napoli N, et al. Diagnosis and management of bone fragility in diabetes: an emerging challenge. Osteoporos Int. 2018; 29: 2585-2596.

[31]

Xu Y, Wu Q. Trends in osteoporosis and mean bone density among type 2 diabetes patients in the US from 2005 to 2014. Sci Rep. 2021; 11: 3693.

[32]

Greco EA, Fornari R, Rossi F, et al. Is obesity protective for osteoporosis? Evaluation of bone mineral density in individuals with high body mass index. Int J Clin Pract. 2010; 64: 817-820.

[33]

Nielson CM, Marshall LM, Adams AL, et al. BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res. 2011; 26: 496-502.

[34]

Kim Y-S, Han JJ, Lee J, Choi HS, Kim JH, Lee T. The correlation between bone mineral density/trabecular bone score and body mass index, height, and weight. Osteoporosis and Sarcopenia. 2017; 3: 98-103.

[35]

Chen L, Liang J, Wen J, et al. Is waist circumference a negative predictor of calcaneal bone mineral density in adult Chinese men with normal weight? Ann Transl Med. 2019; 7: 201.

[36]

Jose A, Cherian KE, Nandyal MB, et al. Trabecular bone score and bone mineral density in postmenopausal women with morbid obesity—a clinical paradox. Med Sci. 2021; 9: 69.

[37]

Behera J, Ison J, Voor MJ, Tyagi N. Probiotics stimulate bone formation in obese mice via histone methylations. Theranostics. 2021; 11: 8605-8623.

[38]

Shu L, Beier E, Sheu T, et al. High-fat diet causes bone loss in young mice by promoting Osteoclastogenesis through alteration of the bone marrow environment. Calcif Tissue Int. 2015; 96: 313-323.

[39]

Kim S, Henneicke H, Cavanagh LL, et al. Osteoblastic glucocorticoid signaling exacerbates high-fat-diet- induced bone loss and obesity. Bone Res. 2021; 9: 40.

[40]

Tsai AG, Bessesen DH. Obesity. Ann Intern Med. 2019; 170: ITC33-ITC46.

[41]

Kumanyika S, Dietz WH. Solving population-wide obesity—Progress and future prospects. N Engl J Med. 2020; 383: 2197-2200.

[42]

Blüher M. Obesity: global epidemiology and pathogenesis. Nat Rev Endocrinol. 2019; 15: 288-298.

[43]

Saeedi P, Petersohn I, Salpea P, et al. Global and regional diabetes prevalence estimates for 2019 and projections for 2030 and 2045: results from the international diabetes federation diabetes atlas. Diabetes Res Clin Pract. 2019; 157: 107843.

[44]

Zhang Y. The epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (COVID-19) in China. Zhonghua Liu Xing Bing Xue Za Zhi. 2020; 41: 145-151.

[45]

Ruan S. Likelihood of survival of coronavirus disease 2019. Lancet Infect Dis. 2020; 20: 630-631.

[46]

Cdc Weekly C. & the novel coronavirus pneumonia emergency response epidemiology team. The epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (COVID-19)—China, 2020. China CDC Weekly. 2020; 2: 113-122.

[47]

Niedźwiedzki T, Filipowska J. Bone remodeling in the context of cellular and systemic regulation: the role of osteocytes and the nervous system. J Mol Endocrinol. 2015; 55: R23-R36.

[48]

Delaisse J-M. The reversal phase of the bone-remodeling cycle: cellular prerequisites for coupling resorption and formation. BoneKEy Reports. 2014; 3: 561.

[49]

Xu X, Chen P, Wang J, et al. Evolution of the novel coronavirus from the ongoing Wuhan outbreak and modeling of its spike protein for risk of human transmission. Sci China Life Sci. 2020; 63: 457-460.

[50]

Lu R, Zhao X, Li J, et al. Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet. 2020; 395: 565-574.

[51]

Zhou P, Yang XL, Wang XG, et al. A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature. 2020; 579: 270-273.

[52]

Burrell LM, Johnston CI, Tikellis C, Cooper ME. ACE2, a new regulator of the renin-angiotensin system. Trends Endocrinol Metab. 2004; 15: 166-169.

[53]

Joshi S, Balasubramanian N, Vasam G, Jarajapu YP. Angiotensin converting enzyme versus angiotensin converting enzyme-2 selectivity of MLN-4760 and DX600 in human and murine bone marrow-derived cells. Eur J Pharmacol. 2016; 774: 25-33.

[54]

Nozato S, Yamamoto K, Takeshita H, et al. Angiotensin 1-7 alleviates aging-associated muscle weakness and bone loss, but is not associated with accelerated aging in ACE2-knockout mice. Clin Sci. 2019; 133: 2005-2018.

[55]

Queiroz-Junior CM, Santos ACPM, Galvão I, et al. The angiotensin converting enzyme 2/angiotensin-(1-7)/mas receptor axis as a key player in alveolar bone remodeling. Bone. 2019; 128: 115041.

[56]

Hasan LK, Deadwiler B, Haratian A, Bolia IK, Weber AE, Petrigliano FA. Effects of COVID-19 on the musculoskeletal system: Clinician's guide. Orr. 2021; 13: 141-150.

[57]

Shimizu H, Nakagami H, Osako MK, et al. Angiotensin II accelerates osteoporosis by activating osteoclasts. FASEB J. 2008; 22: 2465-2475.

[58]

Obitsu S, Ahmed N, Nishitsuji H, et al. Potential enhancement of osteoclastogenesis by severe acute respiratory syndrome coronavirus 3a/X1 protein. Arch Virol. 2009; 154: 1457-1464.

[59]

Li M-Y, Li L, Zhang Y, Wang X-S. Expression of the SARS-CoV-2 cell receptor gene ACE2 in a wide variety of human tissues. Infect Dis Poverty. 2020; 9: 45.

[60]

Mi B, Xiong Y, Zhang C, et al. SARS-CoV-2-induced overexpression of miR-4485 suppresses osteogenic differentiation and impairs fracture healing. Int J Biol Sci. 2021; 17: 1277-1288.

[61]

Gao J, Mei H, Sun J, et al. Neuropilin-1-mediated SARS-CoV-2 infection in bone marrow-derived macrophages inhibits osteoclast differentiation. Advanced Biology. 2022; 6: 2200007.

[62]

Duarte C, Akkaoui J, Ho A, Garcia C, Yamada C, Movila A. Age-dependent effects of the recombinant spike protein/SARS-CoV-2 on the M-CSF- and IL-34-differentiated macrophages in vitro. Biochem Biophys Res Commun. 2021; 546: 97-102.

[63]

Ropa J, Cooper S, Capitano ML, Van't Hof W, Broxmeyer HE. Human hematopoietic stem, progenitor, and immune cells respond ex vivo to SARS-CoV-2 spike protein. Stem Cell Rev Rep. 2021; 17: 253-265.

[64]

Arron JR, Choi Y. Bone versus immune system. Nature. 2000; 408: 535-536.

[65]

Srivastava RK, Dar HY, Mishra PK. Immunoporosis: immunology of osteoporosis—role of T cells. Front Immunol. 2018; 9: 657.

[66]

Ralston SH, Schett G. Osteoimmunology. Calcif Tissue Int. 2018; 102: 501-502.

[67]

Ilesanmi-Oyelere BL, Schollum L, Kuhn-Sherlock B, et al. Inflammatory markers and bone health in postmenopausal women: a cross-sectional overview. Immun Ageing. 2019; 16: 15.

[68]

Fajgenbaum DC, June CH. Cytokine Storm. N Engl J Med. 2020; 383: 2255-2273.

[69]

Hu B, Huang S, Yin L. The cytokine storm and COVID-19. J Med Virol. 2021; 93: 250-256.

[70]

Ye Q, Wang B, Mao J. The pathogenesis and treatment of the ‘cytokine storm’ in COVID-19. J Infect. 2020; 80: 607-613.

[71]

Ragab D, Salah Eldin H, Taeimah M, Khattab R, Salem R. The COVID-19 cytokine storm; what we know so far. Front Immunol. 2020; 11: 1446.

[72]

Choudhary S, Sharma K, Silakari O. The interplay between inflammatory pathways and COVID-19: a critical review on pathogenesis and therapeutic options. Microb Pathog. 2021; 150: 104673.

[73]

Lee J, Park C, Kim HJ, et al. Stimulation of osteoclast migration and bone resorption by C-C chemokine ligands 19 and 21. Exp Mol Med. 2017; 49: e358.

[74]

Okamoto K, Nakashima T, Shinohara M, et al. Osteoimmunology: the conceptual framework unifying the immune and skeletal systems. Physiol Rev. 2017; 97: 1295-1349.

[75]

Hengartner N-E, Fiedler J, Ignatius A, Brenner RE. IL-1β inhibits human osteoblast migration. Mol Med. 2013; 19: 36-42.

[76]

Amarasekara DS, Yu J, Rho J. Bone loss triggered by the cytokine network in inflammatory autoimmune diseases. J Immunol Res. 2015; 2015: 1-12.

[77]

Pathak JL, Bakker AD, Verschueren P, et al. CXCL8 and CCL20 enhance Osteoclastogenesis via modulation of cytokine production by human primary osteoblasts. PLoS One. 2015; 10: e0131041.

[78]

Miyamoto T, Mori T, Yoshimura A, Toyama T. STAT3 is critical to promote inflammatory cytokines and RANKL expression in inflammatory arthritis. Arthritis Res Ther. 2012; 14: P43.

[79]

Li X, Zhou Z, Zhang Y, Yang H. IL-6 contributes to the defective osteogenesis of bone marrow stromal cells from the vertebral body of the glucocorticoid-induced osteoporotic mouse. PLoS One. 2016; 11: e0154677.

[80]

Marahleh A, Kitaura H, Ohori F, et al. TNF-α directly enhances osteocyte RANKL expression and promotes osteoclast formation. Front Immunol. 2019; 10: 2925.

[81]

Luo G, Li F, Li X, Wang Z, Zhang B. TNF-α and RANKL promote osteoclastogenesis by upregulating RANK via the NF-κB pathway. Mol Med Rep. 2018; 17: 6605-6611.

[82]

Song L, Tan J, Wang Z, et al. Interleukin-17A facilitates osteoclast differentiation and bone resorption via activation of autophagy in mouse bone marrow macrophages. Mol Med Rep. 2019; 19: 4743-4752.

[83]

Tang M, Lu L, Yu X. Interleukin-17A interweaves the skeletal and immune systems. Front Immunol. 2021; 11: 625034.

[84]

Lee Y. The role of interleukin-17 in bone metabolism and inflammatory skeletal diseases. BMB Rep. 2013; 46: 479-483.

[85]

Morita T, Shima Y, Fujimoto K, et al. Anti-receptor activator of nuclear factor κB ligand antibody treatment increases osteoclastogenesis-promoting IL-8 in patients with rheumatoid arthritis. Int Immunol. 2019; 31: 277-285.

[86]

Lee J-H, Kim B, Jin WJ, Kim HH, Ha H, Lee ZH. Pathogenic roles of CXCL10 signaling through CXCR3 and TLR4 in macrophages and T cells: relevance for arthritis. Arthritis Res Ther. 2017; 19: 163.

[87]

Niida S, Kaku M, Amano H, et al. Vascular endothelial growth factor can substitute for macrophage Colony-stimulating factor in the support of osteoclastic bone resorption. J Exp Med. 1999; 190: 293-298.

[88]

Niida S, Kondo T, Hiratsuka S, et al. VEGF receptor 1 signaling is essential for osteoclast development and bone marrow formation in colony-stimulating factor 1-deficient mice. Proc Natl Acad Sci USA. 2005; 102: 14016-14021.

[89]

Ratajczak MZ, Bujko K, Ciechanowicz A, et al. SARS-CoV-2 entry receptor ACE2 is expressed on very small CD45−precursors of hematopoietic and endothelial cells and in response to virus spike protein activates the Nlrp3 inflammasome. Stem Cell Rev Rep. 2021; 17: 266-277.

[90]

Rodrigues TS, de Sá KSG, Ishimoto AY, et al. Inflammasomes are activated in response to SARS-CoV-2 infection and are associated with COVID-19 severity in patients. J Exp Med. 2021; 218: e20201707.

[91]

Murakami T, Nakaminami Y, Takahata Y, Hata K, Nishimura R. Activation and function of NLRP3 inflammasome in bone and joint-related diseases. IJMS. 2022; 23: 5365.

[92]

Alippe Y, Wang C, Ricci B, et al. Bone matrix components activate the NLRP3 inflammasome and promote osteoclast differentiation. Sci Rep. 2017; 7: 6630.

[93]

Bonar SL, Brydges SD, Mueller JL, et al. Constitutively activated NLRP3 inflammasome causes inflammation and abnormal skeletal development in mice. PLoS One. 2012; 7: e35979.

[94]

Jiang N, An J, Yang K, et al. NLRP3 inflammasome: a new target for prevention and control of osteoporosis? Front Endocrinol. 2021; 12: 752546.

[95]

Mansoori MN, Shukla P, Kakaji M, et al. IL-18BP is decreased in osteoporotic women: prevents inflammasome mediated IL-18 activation and reduces Th17 differentiation. Sci Rep. 2016; 6: 33680.

[96]

Del Vecchio L, Locatelli F. Hypoxia response and acute lung and kidney injury: possible implications for therapy of COVID-19. Clin Kidney J. 2020; 13: 494-499.

[97]

Galván-Peña S, Leon J, Chowdhary K, et al. Profound Treg perturbations correlate with COVID-19 severity. Proc Natl Acad Sci USA. 2021; 118: e2111315118.

[98]

Rahman A, Tabassum T, Araf Y, al Nahid A, Ullah MA, Hosen MJ. Silent hypoxia in COVID-19: pathomechanism and possible management strategy. Mol Biol Rep. 2021; 48: 3863-3869.

[99]

Dogani B, Månsson F, Resman F, Hartman H, Tham J, Torisson G. The application of an oxygen mask, without supplemental oxygen, improved oxygenation in patients with severe COVID-19 already treated with high-flow nasal cannula. Crit Care. 2021; 25: 319.

[100]

Xiang M, Wu X, Jing H, Novakovic VA, Shi J. The intersection of obesity and (long) COVID-19: hypoxia, thrombotic inflammation, and vascular endothelial injury. Front Cardiovasc Med. 2023; 10: 1062491.

[101]

Chernyak BV, Popova EN, Prikhodko AS, Grebenchikov OA, Zinovkina LA, Zinovkin RA. COVID-19 and oxidative stress. Biochem Mosc. 2020; 85: 1543-1553.

[102]

Hannah SS, McFadden S, McNeilly A, McClean C. “Take my bone away?” hypoxia and bone: a narrative review. J Cell Physiol. 2021; 236: 721-740.

[103]

Ramachandran K. Prevalence of bone mineral density abnormalities and factors affecting bone density in patients with chronic obstructive pulmonary disease in a tertiary Care Hospital in Southern India. JCDR. 2016; 10: OC32-OC34.

[104]

Terzi R, Yılmaz Z. Bone mineral density and changes in bone metabolism in patients with obstructive sleep apnea syndrome. J Bone Miner Metab. 2016; 34: 475-481.

[105]

Rutten EPA, Franssen FME, Spruit MA, Wouters EFM. Anemia is associated with bone mineral density in chronic obstructive pulmonary disease. COPD: J Chron Obstruct Pulmon Dis. 2013; 10: 286-292.

[106]

Cecchini R, Cecchini AL. SARS-CoV-2 infection pathogenesis is related to oxidative stress as a response to aggression. Med Hypotheses. 2020; 143: 110102.

[107]

Doğan S, Pvsn KK, Tomo S, et al. Oxidative stress index can be a new marker related to disease severity in COVID-19. J Trace Elem Med Biol. 2021; 46: 349-357.

[108]

Roessler C, de Oliveira KCS, de Oliveira Portella AX, et al. Evaluation of oxidative stress level: reactive oxygen species, reduced glutathione, and D-dimer in patients hospitalized due to COVID-19. Redox Rep. 2023; 28: 1-6.

[109]

Veenith T, Martin H, le Breuilly M, et al. High generation of reactive oxygen species from neutrophils in patients with severe COVID-19. Sci Rep. 2022; 12: 10484.

[110]

Ahmed SA, Alahmadi YM, Abdou YA. The impact of serum levels of reactive oxygen and nitrogen species on the disease severity of COVID-19. IJMS. 2023; 24: 8973.

[111]

Brandao-Burch A, Utting JC, Orriss IR, Arnett TR. Acidosis inhibits bone formation by osteoblasts in vitro by preventing mineralization. Calcif Tissue Int. 2005; 77: 167-174.

[112]

Wang G, Wang J, Sun D, et al. Short-term hypoxia accelerates bone loss in ovariectomized rats by suppressing osteoblastogenesis but enhancing Osteoclastogenesis. Med Sci Monit. 2016; 22: 2962-2971.

[113]

Apte RS, Chen DS, Ferrara N. VEGF in signaling and disease: beyond discovery and development. Cell. 2019; 176: 1248-1264.

[114]

Ushio-Fukai M. VEGF signaling through NADPH oxidase-derived ROS. Antioxid Redox Signal. 2007; 9: 731-739.

[115]

AbdelMassih A, Yacoub E, Husseiny RJ, et al. Hypoxia-inducible factor (HIF): the link between obesity and COVID-19. Obesity Medicine. 2021; 22: 100317.

[116]

Naidu SAG, Clemens RA, Naidu AS. SARS-CoV-2 infection dysregulates host iron (Fe)-redox homeostasis (Fe-R-H): role of Fe-redox regulators, ferroptosis inhibitors, anticoagulants, and iron-chelators in COVID-19 control. Journal of Dietary Supplements. 2023; 20: 312-371.

[117]

Ding W, Xu C, Zhang Y, Chen H. Advances in the understanding of the role of type-H vessels in the pathogenesis of osteoporosis. Arch Osteoporos. 2020; 15: 5.

[118]

Yuan F-L, Xu MH, Li X, Xinlong H, Fang W, Dong J. The roles of acidosis in osteoclast biology. Front Physiol. 2016; 7: 222.

[119]

Stegen S, Laperre K, Eelen G, et al. HIF-1α metabolically controls collagen synthesis and modification in chondrocytes. Nature. 2019; 565: 511-515.

[120]

Zhang Z, Lai Q, Li Y, et al. Acidic pH environment induces autophagy in osteoblasts. Sci Rep. 2017; 7: 46161.

[121]

Baniasadi M, Talebi S, Mokhtari K, et al. Role of non-coding RNAs in osteoporosis. Pathol Res Pract. 2024; 253: 155036.

[122]

Wierdsma NJ, Kruizenga HM, Konings LAML, et al. Poor nutritional status, risk of sarcopenia and nutrition related complaints are prevalent in COVID-19 patients during and after hospital admission. Clinical Nutrition ESPEN. 2021; 43: 369-376.

[123]

Di Filippo L. COVID-19 is associated with clinically significant weight loss and risk of malnutrition, independent of hospitalisation: a post-hoc analysis of a prospective cohort study. Clin Nutr. 2021; 40: 2420-2426.

[124]

Mohamed DZ, Ghoneim ME-S, Abu-Risha SE-S, Abdelsalam RA, Farag MA. Gastrointestinal and hepatic diseases during the COVID-19 pandemic: manifestations, mechanism and management. WJG. 2021; 27: 4504-4535.

[125]

Muhammad Y et al. Deficiency of antioxidants and increased oxidative stress in COVID-19 patients: a cross-sectional comparative study in Jigawa, northwestern Nigeria. SAGE Open Medicine. 2021; 9: 205031212199124.

[126]

Liu Q, Mak JWY, Su Q, et al. Gut microbiota dynamics in a prospective cohort of patients with post-acute COVID-19 syndrome. Gut. 2022; 71: 544-552.

[127]

Parra-Ortega I, Alcara-Ramírez DG, Ronzon-Ronzon AA, et al. 25-hydroxyvitamin D level is associated with mortality in patients with critical COVID-19: a prospective observational study in Mexico City. Nutr Res Pract. 2021; 15: S32-S40.

[128]

Baktash V, Hosack T, Zahari N, et al. Vitamin D status and outcomes for hospitalised older patients with COVID-19. Postgrad Med J. 2021; 97: 442-447.

[129]

D'Avolio A, Avataneo V, Manca A, et al. 25-hydroxyvitamin D concentrations are lower in patients with positive PCR for SARS-CoV-2. Nutrients. 2020; 12: 1359.

[130]

Lips P, Van Schoor NM. The effect of vitamin D on bone and osteoporosis. Best Pract Res Clin Endocrinol Metab. 2011; 25: 585-591.

[131]

Fan L, Cui Y, Liu Z, et al. Zinc and selenium status in coronavirus disease 2019. Biometals. 2023; 36: 929-941.

[132]

Amin N, Clark CCT, Taghizadeh M, Djafarnejad S. Zinc supplements and bone health: the role of the RANKL-RANK axis as a therapeutic target. J Trace Elem Med Biol. 2020; 57: 126417.

[133]

Zhou Y, Chi J, Lv W, Wang Y. Obesity and diabetes as high-risk factors for severe coronavirus disease 2019 (COVID-19). Diabetes Metab Res Rev. 2021; 37: e3377.

[134]

Aluganti Narasimhulu C, Singla DK. Mechanisms of COVID-19 pathogenesis in diabetes. Am J Physiol Heart Circ Physiol. 2022; 323: H403-H420.

[135]

Zhang J, Ma X, Liu F, et al. Role of NLRP3 inflammasome in diabetes and COVID-19 role of NLRP3 inflammasome in the pathogenesis and treatment of COVID-19 and diabetes NLRP3 inflammasome in diabetes and COVID-19 intervention. Front Immunol. 2023; 14: 1203389.

[136]

Drucker DJ. Diabetes, obesity, metabolism, and SARS-CoV-2 infection: the end of the beginning. Cell Metab. 2021; 33: 479-498.

[137]

Rathinavelu S, Guidry-Elizondo C, Banu J. Molecular modulation of osteoblasts and osteoclasts in type 2 diabetes. J Diabetes Res. 2018; 2018: 6354787.

[138]

Guimarães GC. Obesity, diabetes and risk of bone fragility: how BMAT behavior is affected by metabolic disturbances and its influence on bone health. Osteoporos Int. 2024; 35: 575-588.

[139]

Cândido FG, Bressan J. Vitamin D: link between osteoporosis, obesity, and diabetes? Int J Mol Sci. 2014; 15: 6569-6591.

[140]

Richardson S, Hirsch JS, Narasimhan M, et al. Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized with COVID-19 in the new York City area. JAMA. 2020; 323: 2052-2059.

[141]

Tang J. COVID-19 pandemic and osteoporosis in elderly patients. Aging Dis. 2022; 13: 960-969.

[142]

Awosanya OD, Dadwal UC, Imel EA, Yu Q, Kacena MA. The impacts of COVID-19 on musculoskeletal health. Curr Osteoporos Rep. 2022; 20: 213-225.

[143]

Fumagalli V, Iannacone M. The interplay of drug therapeutics and immune responses to SARS-CoV-2. Cell Mol Immunol. 2024; 21: 197-200.

[144]

Prytula N, Fedotova I, Golbaum M. The possibility of osteoporosis and avascular necrosis caused by the COVID-19 pandemic. Analysis of literature. Orthopaedics traumatology and prosthetics. 2023; 626-627(1-2): 118-122.

[145]

Torres-Naranjo F, de la Peña-Rodríguez P, López-Cervantes RE, et al. Joint position statement on management of patient with osteoporosis during COVID-19 contingency from the AMMOM, CONAMEGER, FELAEN, FEMECOG, FEMECOT, and ICAAFYD. Arch Osteoporos. 2021; 16: 18.

[146]

ATsourdi E, Drake MT. Pros and cons of skeletal medications in the COVID-19 era. Curr Treatm Opt Rheumatol. 2022; 8: 56-69.

[147]

Aspray TJ, Hill TR. In: Harris JR, Korolchuk V, eds. Osteoporosis and the Ageing Skeleton. In Biochemistry and Cell Biology of Ageing: Part II Clinical Science. Singapore: Springer Vol 91; 2019: 453-476.

[148]

Al-Sowayan N. A review on some physiological studies related to osteoporosis. World J Zool. 2014; 9: 214-226.

[149]

Zhang X, Man KW, Li GHY, Tan KCB, Kung AWC, Cheung CL. Osteoporosis is a novel risk factor of infections and sepsis: a cohort study. eClinicalMedicine. 2022; 49: 101488.

[150]

Park SH, Yoon SR, Nam JY, et al. Impact of tuberculosis on the incidence of osteoporosis and osteoporotic fractures: a nationwide population-based cohort study. Public Health. 2023; 216: 13-20.

[151]

Biver E. Osteoporosis and HIV infection. Calcif Tissue Int. 2022; 110: 624-640.

[152]

Upadhyaya GK, Iyengar K, Jain VK, Vaishya R. Challenges and strategies in management of osteoporosis and fragility fracture care during COVID-19 pandemic. J Orthop. 2020; 21: 287-290.

[153]

Boufidou F, Medić S, Lampropoulou V, Siafakas N, Tsakris A, Anastassopoulou C. SARS-CoV-2 reinfections and long COVID in the post-omicron phase of the pandemic. IJMS. 2023; 24: 12962.

[154]

Meng M, Wei R, Wu Y, et al. Long-term risks of respiratory diseases in patients infected with SARS-CoV-2: a longitudinal, population-based cohort study. eClinicalMedicine. 2024; 69: 102500.

[155]

Ma C, Gao J, Liang J, et al. CCL12 induces trabecular bone loss by stimulating RANKL production in BMSCs during acute lung injury. Exp Mol Med. 2023; 55: 818-830.

[156]

Evcik D. Musculoskeletal involvement: COVID-19 and post COVID 19. Turk J Phys Med Rehabil. 2023; 69: 1-7.

[157]

Soares MN, Eggelbusch M, Naddaf E, et al. Skeletal muscle alterations in patients with acute Covid-19 and post-acute sequelae of Covid-19. J Cachexia Sarcopenia Muscle. 2022; 13: 11-22.

[158]

Colosio M, Brocca L, Gatti MF, et al. Structural and functional impairments of skeletal muscle in patients with postacute sequelae of SARS-CoV-2 infection. J Appl Physiol. 2023; 1985(135): 902-917.

[159]

Herrmann M, Engelke K, Ebert R, et al. Interactions between muscle and bone—where physics meets biology. Biomol Ther. 2020; 10: 432.

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