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Serum Uric Acid Concentrations and Risk of Adverse Outcomes in Patients with COVID-19 ORIGINAL RESEARCH published: 06 May 2021 doi: 10.3389/fendo.2021.633767 Serum Uric Acid Concentrations and Risk of Adverse Outcomes in Patients With COVID-19 † † † † † Bo Chen 1 , Chenyang Lu 1 , Hong-Qiu Gu 2,3 , Yang Li 4 , Guqin Zhang 5 , Jonathan Lio 6, Xiongyan Luo 1, Lingshu Zhang 1, Yidan Hu 1, Xiaomeng Lan 7, Zerong Chen 7, Qibing Xie 1* and Huaqin Pan 8,9,10* 1 Department of Rheumatology and Immunology, West China Hospital, Sichuan University, Chengdu, China, 2 China National Clinical Research Center for Neurological Diseases, Beijing Tiantan Hospital, Capital Medical University, Beijing, China, 3 National Center for Healthcare Quality Management in Neurological Diseases, Beijing Tiantan Hospital, Capital Medical University, Beijing, China, 4 Department of Endocrinology, West China Hospital, Sichuan University, Chengdu, China, 5 Department of Respiratory and Critical Care Medicine, Zhongnan Hospital of Wuhan University, Wuhan, China, 6 Internal Medicine, University of Chicago, Chicago, IL, United States, 7 West China School of Public Health and West China Fourth Hospital, Sichuan University, Chengdu, China, 8 Department of Critical Care Medicine, Zhongnan Hospital of Wuhan University, Wuhan, China, 9 Department of Critical Care Medicine, Leishenshan Hospital, Wuhan, China, 10 Clinical Research Edited by: Center of Hubei Critical Care Medicine, Wuhan, China Jeff M. P. Holly, University of Bristol, United Kingdom Background: Although hyperuricemia frequently associates with respiratory diseases, Reviewed by: Yu Sun, patients with severe coronavirus disease 2019 (COVID-19) and severe acute respiratory Shandong University, China syndrome (SARS) can show marked hypouricemia. Previous studies on the association of Ma. Cecilia Opazo, Andres Bello University, Chile serum uric acid with risk of adverse outcomes related to COVID-19 have produced *Correspondence: contradictory results. The precise relationship between admission serum uric acid and Qibing Xie adverse outcomes in hospitalized patients is unknown. [email protected] fi Huaqin Pan Methods: Data of patients affected by laboratory-con rmed COVID-19 and admitted to [email protected] Leishenshan Hospital were retrospectively analyzed. The primary outcome was composite †These authors have contributed and comprised events, such as intensive care unit (ICU) admission, mechanical ventilation, or equally to this work mortality. Logistic regression analysis was performed to explore the association between Specialty section: serum concentrations of uric acid and the composite outcome, as well as each of its This article was submitted to components. To determine the association between serum uric acid and in-hospital Translational Endocrinology, adverse outcomes, serum uric acid was also categorized by restricted cubic spline, and a section of the journal Frontiers in Endocrinology the 95% confidence interval (CI) was used to estimate odds ratios (OR). Received: 26 November 2020 Results: The study cohort included 1854 patients (mean age, 58 years; 52% women). Accepted: 07 April 2021 Published: 06 May 2021 The overall mean ± SD of serum levels of uric acid was 308 ± 96 µmol/L. Among them, 95 Citation: patients were admitted to ICU, 75 patients received mechanical ventilation, and 38 died. In Chen B, Lu C, Gu HQ, Li Y, Zhang G, total, 114 patients reached composite end-points (have either ICU admission, mechanical Lio J, Luo X, Zhang L, Hu Y, Lan X, ventilation or death) during hospitalization. Compared with a reference group with Chen Z, Xie Q and Pan H (2021) ≥ Serum Uric Acid Concentrations estimated baseline serum uric acid of 279-422 µmol/L, serum uric acid values 423 and Risk of Adverse Outcomes µmol/L were associated with an increased risk of composite outcome (OR, 2.60; 95% CI, in Patients With COVID-19. ≤ Front. Endocrinol. 12:633767. 1.07- 6.29) and mechanical ventilation (OR, 3.01; 95% CI, 1.06- 8.51). Serum uric acid doi: 10.3389/fendo.2021.633767 278 µmol/L was associated with an increased risk of the composite outcome (OR, 2.07; Frontiers in Endocrinology | www.frontiersin.org 1 May 2021 | Volume 12 | Article 633767 Chen et al. Uric Acid and COVID-19 95% CI, 1.18- 3.65), ICU admission (OR, 2.18; 95% CI, 1.17- 4.05]), and mechanical ventilation (OR, 2.13; 95% CI, 1.06- 4.28), as assessed by multivariate analysis. Conclusions: This study shows that the association between admission serum uric acid and composite outcome of COVID-19 patients was U-shaped. In particular, we found that compared with baseline serum uric acid levels of 279-422 µmol/L, values ≥ 423 µmol/L were associated with an increased risk of composite outcome and mechanical ventilation, whereas levels ≤ 278 µmol/L associated with increased risk of composite outcome, ICU admission and mechanical ventilation. Keywords: COVID-19, uric acid, relationship, U-shape, adverse outcome INTRODUCTION To date, no evidence on the precise association between serum concentrations of uric acid in COVID-19 patients on admission In December 2019, a cluster of patients with pneumonia, which and in-hospital adverse outcomes exists. In this study, we was later identified as COVID-19, were identified in Wuhan. investigated in detail the relationship between admission serum Thereafter, COVID-19 rapidly spread around the world (1), and, uric acid and the adverse outcomes in hospitalized patients. in November 25, 2020, the World Health Organization reported a total of 46,166,182 confirmed cases globally, with an average mortality being of 2.4% (2). METHODS Patients with COVID-19 present with a variety of signs and symptoms as well as different prognoses, including recovery, Patients admission to the intensive care unit (ICU), the need for This retrospective cohort study included 1854 adult patients mechanical ventilation, and death. Mild cases manifest fever (≥18 years old) admitted to Leishenshan Hospital, a hospital and cough, whereas critical cases may manifest acute respiratory specifically built for COVID-19 treatment during disease distress syndrome (ARDS), sepsis, or septic shock. Early outbreak, between February 16 and April 14, 2020, when the detection of patients who are likely to develop critical disease COVID-19 epidemic occurred in Wuhan (China). The diagnosis is fundamental to identifying high-risk patients and allocating of COVID-19 was confirmed according to the WHO interim limited resources. guidance. SARS-CoV-2 positivity was diagnosed by real-time A high incidence of renal abnormalities and gastrointestinal reverse-transcriptase polymerase-chain-reaction (RT-PCR) symptoms has been reported in patients with COVID-19, and assay conducted on nasal and pharyngeal swab specimens. kidney diseases are frequently associated with mortality in these Patients with incomplete or missing serum uric acid values patients (3–6). The kidneys and gut are both targets of SARS- within 24 hours after admission were excluded (n = 14). CoV-2 and the primary sites of uric acid excretion. Therefore, it Patients with chronic kidney disease, gout, chronic liver disease is likely that infection with SARS-CoV-2 could affect regulation with severe liver dysfunction, or malignancies (n = 50) were also of uric acid metabolism and levels in the serum. Indeed, studies excluded from the study. The flowchart of participants’ progress have shown that serum uric acid concentrations were markedly through the study is shown in Supplementary Figure S1. lower in patients with severe COVID-19 disease (7–9), which Clinical data of all COVID-19 patients were collected. Due to may be caused by decreased net renal tubular reabsorption of the outbreak of the COVID-19 epidemic, written informed uric acid due to inflammation. In SARS-CoV-2-affected patients, consent could not be collected from patients. We only made hypouricemia was also found to be strongly associated with a use of the deidentified retrospective data in this study. In poor prognosis (10). However, hyperuricemia is known to be addition, our study has been approved by the Ethics associated with hypoxia and systemic inflammation in Committee of the Zhongnan Hospital of Wuhan University. respiratory diseases (11). Angiotensin converting enzyme 2 (ACE2), the receptor for the entry of SARS-CoV-2, is strongly Baseline Measurements and Definition expressed in the kidney (12, 13), and SARS-CoV-2 can be Relevant patients’ characteristics were recorded from electronic detected in COVID-19 patients’ urine (14, 15). COVID-19- medical records, including age, sex, and comorbidities. Clinical associated nephritis, which manifests as leukocyturia, and laboratory data were obtained within the first 24 hours of albuminuria, and hematuria, is considered an early indicator of admission. They included vital signs, long-term use of disease severity (16). Furthermore, a single-cell analysis showed medications, mode of respiratory support, complete blood enriched expression of ACE2 in all subtypes of proximal tubular count, coagulation profile, serum uric acid, creatinine, cells of the kidney (13), which are the most important regulators electrolytes, renal and liver function, lactate dehydrogenase, of serum urate (17). A recent study also observed that uric acid and D-dimer concentrations. Outcome data were also collected significantly increases in children with severe COVID-19 from electronic medical records. The Leishenshan hospital was compared with non-severe children on admission (18). closed on April 14, enabling complete extraction of outcome Frontiers in Endocrinology | www.frontiersin.org 2 May 2021 | Volume
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