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Alsunaid A, Spencer S, Bhandari S. Intravenous iron in chronic kidney disease without anaemia but iron deficiency: A scoping review. World J Nephrol 2025; 14:101576. [PMID: 40134647 PMCID: PMC11755244 DOI: 10.5527/wjn.v14.i1.101576] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 09/19/2024] [Revised: 12/30/2024] [Accepted: 01/09/2025] [Indexed: 01/20/2025] Open
Abstract
Iron deficiency (ID) is a prevalent complication of chronic kidney disease (CKD), often managed reactively when associated with anaemia. This scoping review evaluates the evidence supporting intravenous (IV) iron therapy in non-anaemic individuals with CKD and ID, focusing on safety, efficacy, and emerging therapeutic implications. Current diagnostic markers, including serum ferritin, transferrin saturation, and reticulocyte haemoglobin content, are reviewed alongside their limitations in the context of inflammation and variability. The pathophysiology of ID in CKD is explored, highlighting the roles of hepcidin, hypoxia-inducible factor pathways, and uraemic toxins. Comparative studies reveal that IV iron offers a more rapid correction of iron stores, improved compliance, and fewer gastrointestinal side effects compared to oral iron. Evidence from trials such as "iron and heart" and "iron and muscle" suggests potential benefits of IV iron on functional capacity and fatigue, though findings were statistically non-significant. Insights from heart failure trials support the safety and efficacy of IV iron in improving quality of life and reducing hospitalizations, with newer formulations like ferric derisomaltose demonstrating favourable safety profiles. This review underscores the need for standardized screening protocols for ID in CKD, even in the absence of anaemia, to facilitate earlier intervention. Future research should prioritise robust outcome measures, larger sample sizes, and person-specific treatment strategies to optimise dosing and administration frequency. Tailored approaches to IV iron therapy have the potential to significantly improve functional outcomes, quality of life, and long-term health in people with CKD.
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Affiliation(s)
- Abdulrahman Alsunaid
- Department of Medical Science, Hull York Medical School, Kingston Upon Hull HU6 7RU, United Kingdom
| | - Sebastian Spencer
- Department of Medical Science, Hull York Medical School, Kingston Upon Hull HU6 7RU, United Kingdom
- Department of Medical Science, University of Hull, Kingston Upon Hull HU6 7RU, United Kingdom
- Department of Academic Renal, Hull University Teaching Hospitals NHS Trust, Kingston Upon Hull HU3 2JZ, United Kingdom
| | - Sunil Bhandari
- Department of Medical Science, Hull York Medical School, Kingston Upon Hull HU6 7RU, United Kingdom
- Department of Academic Renal, Hull University Teaching Hospitals NHS Trust, Kingston Upon Hull HU3 2JZ, United Kingdom
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Zhao B, Yang X, Li W, Zhu H, Meng Q, Ma Y, Liu Y, Zhou Y, Lin J, Zhai C, Zhao L, Sun J, Wang R. Effect of roxadustat on red blood cell lifespan in patients with long-term haemodialysis: a single-centre, prospective, single-arm study. Clin Kidney J 2023; 16:1500-1507. [PMID: 37664567 PMCID: PMC10469108 DOI: 10.1093/ckj/sfad080] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [Key Words] [Grants] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 11/23/2022] [Indexed: 09/05/2023] Open
Abstract
Background Reduced survival of red blood cells (RBCs) in patients with chronic kidney disease (CKD) is thought to contribute to renal anaemia. Although renal anaemia improved greatly because of the wide use of erythropoiesis-stimulating agents (ESAs) and the advancement of dialysis techniques, RBC longevity seems not to be obviously ameliorated. Methods In this single-centre, single-arm trial, patients who had been undergoing haemodialysis and ESA therapy with epoetin alfa for at least 12 weeks changed their anti-anaemia drugs from epoetin alfa to oral roxadustat three times per week for 24 weeks. The primary endpoint was the change in RBC lifespan from baseline at week 24. The change in the circulating percentage of eryptotic RBCs, RBC deformability and RBC oxygen transport ability were also assessed. Results A total of 27 patients were enrolled, with 26 completing the full course of intervention. At baseline, the average RBC lifespan was 60.1 days [standard deviation (SD) 14.4; n = 27]. At the end of the study period, 26 patients had an RBC lifespan measurement (83.9 days on average; SD 21.9). The RBC lifespan increased by 22.8 days on average [95% confidence interval (CI) 15.5-30.0, P < .001]. This equated to an average RBC lifespan increase of 39.2% (95% CI 27.8-50.6). The percentage of circulating eryptotic RBCs, erythrocyte filtration index and the pressure at which haemoglobin is 50% saturated decreased significantly from baseline to week 24 (1.39 ± 0.44% versus 0.89 ± 0.25%, P < .0001; 0.29 ± 0.12 versus 0.16 ± 0.08, P < .0001 and 32.54 ± 4.83 versus 28.40 ± 2.29, P < .001, respectively). Conclusion Roxadustat prolonged RBC lifespan in patients with long-term haemodialysis.
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Affiliation(s)
- Bing Zhao
- Department of Nephrology, Shandong Provincial Hospital affiliated to Shandong First Medical University, Jinan, Shandong, China
| | - Xiaowei Yang
- Department of Nephrology, Shandong Provincial Hospital affiliated to Shandong First Medical University, Jinan, Shandong, China
| | - Weidan Li
- Institute of Health Service and Transfusion Medicine, Academy of Military Medical Sciences, Academy of Military Science of the Chinese People's Liberation Army, Beijing, China
| | - Huizi Zhu
- Department of Nephrology, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, China
| | - Qian Meng
- Department of Nephrology, Shandong Provincial Hospital affiliated to Shandong First Medical University, Jinan, Shandong, China
| | - Yongjian Ma
- Guangdong Breath Test Engineering and Technology Research Center, Shenzhen University, Shenzhen, China
| | - Yun Liu
- Department of Clinical Laboratory, Shandong Provincial Hospital affiliated to Shandong First Medical University, Jinan, Shandong, China
| | - Yan Zhou
- Department of Nephrology, Shandong Provincial Hospital affiliated to Shandong First Medical University, Jinan, Shandong, China
| | - Jiangong Lin
- Department of Nephrology, Shandong Provincial Hospital affiliated to Shandong First Medical University, Jinan, Shandong, China
| | - Chunjuan Zhai
- Department of Cardiology Shandong Provincial Hospital affiliated to Shandong First Medical University, Jinan, Shandong, China
| | - Lian Zhao
- Institute of Health Service and Transfusion Medicine, Academy of Military Medical Sciences, Academy of Military Science of the Chinese People's Liberation Army, Beijing, China
| | - Jing Sun
- Department of Nephrology, Shandong Provincial Hospital affiliated to Shandong First Medical University, Jinan, Shandong, China
- Department of Nephrology, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, China
| | - Rong Wang
- Department of Nephrology, Shandong Provincial Hospital affiliated to Shandong First Medical University, Jinan, Shandong, China
- Department of Nephrology, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong, China
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Zeng L, Chan GCK, Ng JKC, Fung WWS, Chow KM, Szeto CC. The effect of Dipeptidyl peptidase 4 (DPP-4) inhibitors on hemoglobin level in diabetic kidney disease: A retrospective cohort study. Medicine (Baltimore) 2023; 102:e34538. [PMID: 37565855 PMCID: PMC10419505 DOI: 10.1097/md.0000000000034538] [Citation(s) in RCA: 0] [Impact Index Per Article: 0] [Reference Citation Analysis] [Abstract] [MESH Headings] [Track Full Text] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 04/26/2023] [Accepted: 07/11/2023] [Indexed: 08/12/2023] Open
Abstract
Anemia typically develops early in the course of diabetic kidney disease (DKD). There are data to show that dipeptidyl-peptidase-4 (DPP-4) inhibitors affect hematopoietic growth factor activity and hemoglobin level. We retrospectively reviewed 443 DKD patients who were started on DDP-4 inhibitor therapy in 2019. Their hemoglobin level at baseline (6-12 months before treatment), pretreatment (0-6 months before treatment), and post-treatment periods (within 6 months after DPP-4 inhibitor), concomitant estimated glomerular filtration rate (eGFR), HbA1c, peripheral blood white cell and platelet counts were reviewed. The severity of kidney failure was classified according to the Kidney Disease: Improving Global Outcomes stages. The hemoglobin level had a small but significant decline from 11.98 ± 2.07 to 11.87 ± 2.12 g/dL from pretreatment to post-treatment period (paired Student t test, P < .0001). From the pre- to post-treatment period, the decline of hemoglobin level was 0.10 ± 0.89 g/dL, which was significantly less than that from baseline to pretreatment period (0.24 ± 0.90 g/dL, P = .0008). The change in hemoglobin level had a positive correlation with the change in HbA1c level (R = 0.218, P < .0001), but did not correlate with the type of DPP-4 inhibitor or pretreatment eGFR. There was no significant change in peripheral blood white cell or platelet count during the same period. DPP-4 inhibitor ameliorates hemoglobin decline in DKD. The effect of DPP-4 inhibitor on hemoglobin is statistically significant but clinically modest, and did not correlate with the concomitant change in kidney function.
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Affiliation(s)
- Lingfeng Zeng
- Carol & Richard Yu Peritoneal Dialysis Research Centre, Department of Medicine & Therapeutics, Prince of Wales Hospital, Shatin, Hong Kong, China
- Li Ka Shing Institute of Health Sciences (LiHS), Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong, China
| | - Gordon C K Chan
- Carol & Richard Yu Peritoneal Dialysis Research Centre, Department of Medicine & Therapeutics, Prince of Wales Hospital, Shatin, Hong Kong, China
| | - Jack K C Ng
- Carol & Richard Yu Peritoneal Dialysis Research Centre, Department of Medicine & Therapeutics, Prince of Wales Hospital, Shatin, Hong Kong, China
| | - Winston W S Fung
- Carol & Richard Yu Peritoneal Dialysis Research Centre, Department of Medicine & Therapeutics, Prince of Wales Hospital, Shatin, Hong Kong, China
| | - Kai-Ming Chow
- Carol & Richard Yu Peritoneal Dialysis Research Centre, Department of Medicine & Therapeutics, Prince of Wales Hospital, Shatin, Hong Kong, China
| | - Cheuk-Chun Szeto
- Carol & Richard Yu Peritoneal Dialysis Research Centre, Department of Medicine & Therapeutics, Prince of Wales Hospital, Shatin, Hong Kong, China
- Li Ka Shing Institute of Health Sciences (LiHS), Faculty of Medicine, The Chinese University of Hong Kong, Shatin, Hong Kong, China
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Kan C, Lu X, Zhang R. Effects of hypoxia on bone metabolism and anemia in patients with chronic kidney disease. World J Clin Cases 2021; 9:10616-10625. [PMID: 35004993 PMCID: PMC8686129 DOI: 10.12998/wjcc.v9.i34.10616] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Download PDF] [Journal Information] [Submit a Manuscript] [Subscribe] [Scholar Register] [Received: 05/07/2021] [Revised: 08/12/2021] [Accepted: 10/25/2021] [Indexed: 02/06/2023] Open
Abstract
BACKGROUND Abnormal bone metabolism and renal anemia seriously affect the prognosis of patients with chronic kidney disease (CKD). Existing studies have mostly addressed the pathogenesis and treatment of bone metabolism abnormality and anemia in patients with CKD, but few have evaluated their mutual connection. Administration of exogenous erythropoietin to CKD patients with anemia used to be the mainstay of therapeutic approaches; however, with the availability of hypoxia-inducible factor (HIF) stabilizers such as roxadustat, more therapeutic choices for renal anemia are expected in the future. However, the effects posed by the hypoxic environment on both CKD complications remain incompletely understood. AIM To summarize the relationship between renal anemia and abnormal bone metabolism, and to discuss the influence of hypoxia on bone metabolism. METHODS CNKI and PubMed searches were performed using the key words "chronic kidney disease," "abnormal bone metabolism," "anemia," "hypoxia," and "HIF" to identify relevant articles published in multiple languages and fields. Reference lists from identified articles were reviewed to extract additional pertinent articles. Then we retrieved the Abstract and Introduction and searched the results from the literature, classified the extracted information, and summarized important information. Finally, we made our own conclusions. RESULTS There is a bidirectional relationship between renal anemia and abnormal bone metabolism. Abnormal vitamin D metabolism and hyperparathyroidism can affect bone metabolism, blood cell production, and survival rates through multiple pathways. Anemia will further attenuate the normal bone growth. The hypoxic environment regulates bone morphogenetic protein, vascular endothelial growth factor, and neuropilin-1, and affects osteoblast/osteoclast maturation and differentiation through bone metabolic changes. Hypoxia preconditioning of mesenchymal stem cells (MSCs) can enhance their paracrine effects and promote fracture healing. Concurrently, hypoxia reduces the inhibitory effect on osteocyte differentiation by inhibiting the expression of fibroblast growth factor 23. Hypoxia potentially improves bone metabolism, but it still carries potential risks. The optimal concentration and duration of hypoxia remain unclear. CONCLUSION There is a bidirectional relationship between renal anemia and abnormal bone metabolism. Hypoxia may improve bone metabolism but the concentration and duration of hypoxia remain unclear and need further study.
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Affiliation(s)
- Chao Kan
- Department of Clinical Medicine, Changchun University of Chinese Medicine, Changchun 130000, Jilin Province, China
| | - Xu Lu
- Department of Clinical Medicine, Changchun University of Chinese Medicine, Changchun 130000, Jilin Province, China
| | - Rui Zhang
- Department of Nephrology, Zhuhai People’s Hospital (Zhuhai Hospital Affiliated with Jinan University), Zhuhai 519070, Guangdong Province, China
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Chen J, Li Z, Zhang H, Hu J, Wang J, Zhou H, Liu Y, Liu J, Yi B, Zhang W. A Prospective, Self-Controlled Pilot Study of the Efficacy of Roxadustat for Erythropoietin Hyporesponsiveness in Patients Requiring Chronic Ambulatory Peritoneal Dialysis. J Ren Nutr 2021; 32:595-604. [PMID: 34756787 DOI: 10.1053/j.jrn.2021.09.003] [Citation(s) in RCA: 2] [Impact Index Per Article: 0.5] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/26/2021] [Revised: 08/20/2021] [Accepted: 09/05/2021] [Indexed: 02/08/2023] Open
Abstract
OBJECTIVES The present study aimed to explore the efficacy and safety of roxadustat in patients with renal anemia and erythropoietin (EPO) hyporesponsive who are receiving continuous ambulatory peritoneal dialysis (CAPD). METHODS This is a single center, before and after treatment, self-controlled study; 55 CAPD patients with renal anemia and EPO hyporesponsiveness were enrolled. The main follow-up parameters included routine blood, liver and kidney function, electrolyte, blood lipid, high-sensitivity C-reactive protein, and iron tests. Serum samples were used to determine interleukin-6 and tumor necrosis factor-α levels via enzyme linked immunosorbent assay. The Modified Quantitative Subjective Global Assessment Score and Malnutrition-Inflammation Score before and after treatment, and adverse events during treatment were recorded. The follow-up observation time was 12 weeks. Preliminary data 12-24 weeks before the enrollment as well as post-follow-up data at 36 weeks were also collected. RESULTS Fifty patients completed the 12-week follow-up. The hemoglobin levels were 8.0 ± 1.2 g/dL at baseline and 11.2 ± 2.0 g/dL after 12 weeks of roxadustat treatment. The hemoglobin increases at all measured time points and was statistically significant compared with the baseline value (P < .05). The overall hemoglobin response rate (hemoglobin increase ≥ 1.0 g/dL) was 80%, and 50% of the patients reached the hemoglobin target (hemoglobin ≥ 11.0 g/dL) at 12 weeks. Transferrin was higher at 12 weeks (2.2 ± 0.5 g/L) than at baseline (1.7 ± 0.5 g/L) (P < .05), while serum ferritin levels slightly decreased compared with the baseline value (P > .05). The median high-sensitivity C-reactive protein level and other inflammation-related indicators, such as white blood cell counts, neutrophil-to-lymphocyte ratio, platelet-to-lymphocyte ratio, interleukin-6, and tumor necrosis factor-α, were not significantly different from their baseline values. Nutrition-related biochemical indices such as albumin, creatinine, and blood lipids were also not significantly changed. The Modified Quantitative Subjective Global Assessment Score and Malnutrition-Inflammation Score were slightly lower at 12 weeks than at baseline. No serious adverse events were observed during the follow-up period. Post-follow-up data revealed a maintained hemoglobin level in patients who remained on roxadustat treatment while those switched back to EPO treatment after 12 weeks resulted in a decreased hemoglobin at 36 weeks. CONCLUSIONS In patients with EPO hyporesponsiveness on CAPD, roxadustat can efficiently and safely improve anemia and nutritional status without promoting inflammation.
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Affiliation(s)
- Junjie Chen
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China
| | - Zhi Li
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China
| | - Hao Zhang
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China.
| | - Jing Hu
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China
| | - Jianwen Wang
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China
| | - Huang Zhou
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China
| | - Yan Liu
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China
| | - Jun Liu
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China
| | - Bin Yi
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China
| | - Wei Zhang
- Department of Nephrology, The Third Xiangya Hospital, Central South University, Changsha, Hunan Province, China.
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Bissinger R, Nemkov T, D'Alessandro A, Grau M, Dietz T, Bohnert BN, Essigke D, Wörn M, Schaefer L, Xiao M, Beirne JM, Kalo MZ, Schork A, Bakchoul T, Omage K, Kong L, Gonzalez-Menendez I, Quintanilla-Martinez L, Fehrenbacher B, Schaller M, Dhariwal A, Birkenfeld AL, Grahammer F, Qadri SM, Artunc F. Proteinuric chronic kidney disease is associated with altered red blood cell lifespan, deformability and metabolism. Kidney Int 2021; 100:1227-1239. [PMID: 34537228 DOI: 10.1016/j.kint.2021.08.024] [Citation(s) in RCA: 32] [Impact Index Per Article: 8.0] [Reference Citation Analysis] [Abstract] [Key Words] [Track Full Text] [Journal Information] [Subscribe] [Scholar Register] [Received: 03/03/2021] [Revised: 08/05/2021] [Accepted: 08/13/2021] [Indexed: 12/14/2022]
Abstract
Anemia is a common complication of chronic kidney disease, affecting the quality of life of patients. Among various factors, such as iron and erythropoietin deficiency, reduced red blood cell (RBC) lifespan has been implicated in the pathogenesis of anemia. However, mechanistic data on in vivo RBC dysfunction in kidney disease are lacking. Herein, we describe the development of chronic kidney disease-associated anemia in mice with proteinuric kidney disease resulting from either administration of doxorubicin or an inducible podocin deficiency. In both experimental models, anemia manifested at day 10 and progressed at day 30 despite increased circulating erythropoietin levels and erythropoiesis in the bone marrow and spleen. Circulating RBCs in both mouse models displayed altered morphology and diminished osmotic-sensitive deformability together with increased phosphatidylserine externalization on the outer plasma membrane, a hallmark of RBC death. Fluorescence-labelling of RBCs at day 20 of mice with doxorubicin-induced kidney disease revealed premature clearance from the circulation. Metabolomic analyses of RBCs from both mouse models demonstrated temporal changes in redox recycling pathways and Lands' cycle, a membrane lipid remodeling process. Anemic patients with proteinuric kidney disease had an increased proportion of circulating phosphatidylserine-positive RBCs. Thus, our observations suggest that reduced RBC lifespan, mediated by altered RBC metabolism, reduced RBC deformability, and enhanced cell death contribute to the development of anemia in proteinuric kidney disease.
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Affiliation(s)
- Rosi Bissinger
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany
| | - Travis Nemkov
- Department of Biochemistry and Molecular Genetics, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA
| | - Angelo D'Alessandro
- Department of Biochemistry and Molecular Genetics, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA; Division of Hematology, University of Colorado Denver, Aurora, Colorado, USA
| | - Marijke Grau
- Institute of Molecular and Cellular Sports Medicine, German Sport University of Cologne, Köln, Germany
| | - Thomas Dietz
- Institute of Molecular and Cellular Sports Medicine, German Sport University of Cologne, Köln, Germany
| | - Bernhard N Bohnert
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany; Institute of Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD) at the University Tübingen, Tübingen, Germany
| | - Daniel Essigke
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany
| | - Matthias Wörn
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany
| | - Lina Schaefer
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany
| | - Mengyun Xiao
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany
| | - Jonathan M Beirne
- Department of Biochemistry and Molecular Genetics, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA
| | - M Zaher Kalo
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany
| | - Anja Schork
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany; Institute of Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD) at the University Tübingen, Tübingen, Germany
| | - Tamam Bakchoul
- Center for Clinical Transfusion Medicine, University Hospital of Tübingen, Tübingen, Germany
| | - Kingsley Omage
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany
| | - Lingsi Kong
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany
| | | | | | - Birgit Fehrenbacher
- Department of Dermatology, Eberhard Karls University Tübingen, Tübingen, Germany
| | - Martin Schaller
- Department of Dermatology, Eberhard Karls University Tübingen, Tübingen, Germany
| | - Achal Dhariwal
- Institute of Oral Biology, Faculty of Dentistry, University of Oslo, Oslo, Norway
| | - Andreas L Birkenfeld
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany; Institute of Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD) at the University Tübingen, Tübingen, Germany
| | - Florian Grahammer
- Department of Medicine, University Medical Center Hamburg-Eppendorf, Hamburg, Germany
| | - Syed M Qadri
- Faculty of Health Sciences, Ontario Tech University, Oshawa, Ontario, Canada
| | - Ferruh Artunc
- Division of Endocrinology, Diabetology and Nephrology, Department of Internal Medicine, University Hospital Tübingen, Tübingen, Germany; Institute of Diabetes Research and Metabolic Diseases (IDM) of the Helmholtz Center Munich at the University Tübingen, Tübingen, Germany; German Center for Diabetes Research (DZD) at the University Tübingen, Tübingen, Germany.
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