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Relation of Serum Copper Status to Survival in COVID-19

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Relation of Serum Copper Status to Survival in COVID-19 nutrients Article Relation of Serum Copper Status to Survival in COVID-19 Julian Hackler 1, Raban Arved Heller 1,2,3 , Qian Sun 1 , Marco Schwarzer 4, Joachim Diegmann 4, Manuel Bachmann 4, Arash Moghaddam 5 and Lutz Schomburg 1,* 1 Institute for Experimental Endocrinology, Charité-Universitätsmedizin Berlin, Corporate Member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, D-10115 Berlin, Germany; [email protected] (J.H.); [email protected] (R.A.H.); [email protected] (Q.S.) 2 Bundeswehr Hospital Berlin, Clinic of Traumatology and Orthopaedics, D-10115 Berlin, Germany 3 Department of General Practice and Health Services Research, Heidelberg University Hospital, D-69120 Heidelberg, Germany 4 ATORG, Center for Orthopaedics, Aschaffenburg Trauma and Orthopaedic Research Group, Trauma Surgery and Sports Medicine, Hospital Aschaffenburg-Alzenau, D-63739 Aschaffenburg, Germany; [email protected] (M.S.); [email protected] (J.D.); [email protected] (M.B.) 5 Orthopedic and Trauma Surgery, Frohsinnstraße 12, D-63739 Aschaffenburg, Germany; [email protected] * Correspondence: [email protected]; Tel.: +49-30-450524289; Fax: +49-30-4507524289 Abstract: The trace element copper (Cu) is part of our nutrition and essentially needed for several cuproenzymes that control redox status and support the immune system. In blood, the ferroxidase ceruloplasmin (CP) accounts for the majority of circulating Cu and serves as transport protein. Both Cu and CP behave as positive, whereas serum selenium (Se) and its transporter selenoprotein P (SELENOP) behave as negative acute phase reactants. In view that coronavirus disease (COVID-19) causes systemic inflammation, we hypothesized that biomarkers of Cu and Se status are regulated Citation: Hackler, J.; Heller, R.A.; inversely, in relation to disease severity and mortality risk. Serum samples from COVID-19 patients Sun, Q.; Schwarzer, M.; Diegmann, J.; were analysed for Cu by total reflection X-ray fluorescence and CP was quantified by a validated Bachmann, M.; Moghaddam, A.; sandwich ELISA. The two Cu biomarkers correlated positively in serum from patients with COVID- Schomburg, L. Relation of Serum 19 (R = 0.42, p < 0.001). Surviving patients showed higher mean serum Cu and CP concentrations Copper Status to Survival in in comparison to non-survivors ([mean+/−SEM], Cu; 1475.9+/−22.7 vs. 1317.9+/−43.9 µg/L; COVID-19. Nutrients 2021, 13, 1898. − − https://doi.org/10.3390/nu13061898 p < 0.001, CP; 547.2.5+/ 19.5 vs. 438.8+/ 32.9 mg/L, p = 0.086). In contrast to expectations, total serum Cu and Se concentrations displayed a positive linear correlation in the patient samples Academic Editor: Catherine analysed (R = 0.23, p = 0.003). Serum CP and SELENOP levels were not interrelated. Applying L. Carpenter receiver operating characteristics (ROC) curve analysis, the combination of Cu and SELENOP with age outperformed other combinations of parameters for predicting risk of death, yielding an AUC of Received: 29 April 2021 95.0%. We conclude that the alterations in serum biomarkers of Cu and Se status in COVID-19 are not Accepted: 30 May 2021 compatible with a simple acute phase response, and that serum Cu and SELENOP levels contribute Published: 31 May 2021 to a good prediction of survival. Adjuvant supplementation in patients with diagnostically proven deficits in Cu or Se may positively influence disease course, as both increase in survivors and are of Publisher’s Note: MDPI stays neutral crucial importance for the immune response and antioxidative defence systems. with regard to jurisdictional claims in published maps and institutional affil- Keywords: trace element; inflammation; ceruloplasmin; micronutrient; COVID-19 iations. 1. Introduction Copyright: © 2021 by the authors. The immune system relies on a sufficiently high supply of micronutrients in order Licensee MDPI, Basel, Switzerland. to fulfil its essential functions in surveillance and defense. Certain vitamins and trace This article is an open access article elements are assumed to play a key role in coping with the coronavirus disease (COVID-19) distributed under the terms and conditions of the Creative Commons caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), including Attribution (CC BY) license (https:// vitamin D and C, along with the essential trace elements copper (Cu), selenium (Se) and creativecommons.org/licenses/by/ zinc (Zn) [1,2]. Despite a number of insightful and thought-provoking recent reviews and 4.0/). Nutrients 2021, 13, 1898. https://doi.org/10.3390/nu13061898 https://www.mdpi.com/journal/nutrients Nutrients 2021, 13, 1898 2 of 12 hypotheses on the potentially underlying mechanisms of interrelation, laboratory analyses and clinical studies are few and the respective database is limited. The inconclusive knowledge is probably reflected best in the discussions on a potential role of vitamin D in COVID-19 [3–5]. While there is some consensus that vitamin D con- centrations are decreased, it is unclear whether supplementation would be beneficial [6–8]. The observed deficiency in COVID-19 may result from its downregulation in response to systemic inflammation [9]. The same applies to the essential trace elements Se and Zn, where supplementation studies are suggested in order to correcting the observed deficiencies in COVID-19 [10–12]. The rationale for this hypothesis is mainly based on two fundamental findings, i.e., the general notion of a dysfunctional immune system in Se or Zn deficiency [13,14], and a depressed Se or Zn concentration observed in inflammatory or severe diseases [15–17]. The detected decline in the circulating concentration of Se and Zn may reflect a meaningful adaptation of the organism to the infection as part of the anti-viral response, but it is also of relevance to target tissues relying on a sufficiently high supply. Consequently, both circulating and target tissue deficits may result, collectively causing a depressed trace element status, whereby “status” denotes a concept encompassing intake, metabolism and reserves of an essential micronutrient [18,19]. As intracellular and circulating con- centrations are interrelated and the latter only are accessible for analytical monitoring, circulating parameters are established as biomarkers of trace element status [20–23]. The Se transporter selenoprotein P (SELENOP) along with glutathione peroxidase-3 and total serum Se concentrations are established biomarkers of Se status [22–24], whereas serum Cu along with ceruloplasmin (CP) concentrations serve as readily available biomarkers of Cu status [25–27]. In the case of Se, COVID-19 cure rates were associated with Se status in different populations of China with varying habitual intake levels [28], and disease severity along with mortality risk were directly correlated to Se deficiency in laboratory analyses of individual patients [29–31]. Together with the knowledge on an increased mutation rate of virus species in a Se-deprived host organism [32], and the generally increased risk of disease-related death in Se deficiency [20], it appears prudent to avoid Se deficiency as a meaningful preventive measure. Whether supplemental Se will yield positive health effects in COVID-19 remains to be studied. The data base on Zn in COVID-19 is similarly limited, and low Zn concentrations are observed in severely diseased patients [33,34]. In contrast to the declining Se status in non-surviving patients, serum Zn levels seem to recover in COVID-19 during the hospital stay, indicative of a redistribution between circulation and immune cells [29]. Similar to Se and Zn, the essential trace element Cu is also needed for a regular immune response. A number of catalytically active cuproenzymes affect general developmental as well as metabolic and adaptive pathways [35,36]. Accordingly, a systemic deficiency in Cu is associated with a number of diverse symptoms that are related to Cu-containing enzymes, e.g., incomplete collagen formation, pigmentation defects, catecholamine misbalance and impaired neuronal signalling as well as muscle weakness and cardiomyopathy, partly due to insufficient biosynthesis of lysyl-oxidase, dopamine beta-hydrolase and cytochrome c oxidase, respectively [37–39]. In addition, severe hematologic and neurologic symptoms develop under conditions of chronic Cu deficiency [40–42]. Inherited defects in key genes of Cu transport cause childhood-onset and potentially fatal Cu deficiency with severe and life-threatening neurological defects, as observed in Menkes disease with mutations in the intracellular Cu-transporter ATP7A [43]. Under regular conditions, severe changes in Cu metabolism are observed in response to inflammation, where serum Cu and CP behave as positive acute phase reactants, i.e., in opposite direction to serum Se and SELENOP [44–46]. For these reasons, we decided to determine Cu and CP in relation to biomarkers of Se status in serum of patients with COVID-19, and to test their value for predicting survival odds. Nutrients 2021, 13, 1898 3 of 12 2. Materials and Methods 2.1. Study Design Longitudinal serum samples were available from a cross-sectional study of surviv- ing and non-surviving patients with COVID-19, who were hospitalized at Klinikum Aschaffenburg-Alzenau in Germany, as described earlier [30]. The study was conducted in accordance with the Declaration of Helsinki. Ethical counselling had been obtained from the authorities in Bavaria, Germany (Ethik-Kommission der Bayerischen
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