Prognostic Significance of Risk Factors and Biomarkers in Patients Hospitalized for Cardiorenal Syndromes: A Pilot Study

Page: [492 - 507] Pages: 16

  • * (Excluding Mailing and Handling)

Abstract

Background: Cardiorenal syndromes (CRS), involving the heart-kidney cross-talk and the activation of neurohumoral and inflammatory pathways, are an entity characterized by high morbidity and mortality.

Objective: To evaluate the prognostic role of risk factors and biomarkers in patients hospitalized for CRS.

Methods: In this observational cohort study, 100 consecutive patients hospitalized for CRS were enrolled. Socio-demographic characteristics, personal medical history, and prior medication use were recorded upon admission, and echocardiography was performed. Moreover, an array of blood markers were measured. The endpoint of interest was a composite of death or dialysis dependence at discharge.

Results: Patients were classified into two groups; Group 1 (N= 52): discharged being dialysis-independent, Group 2 (N=48): death/dialysis dependence at discharge. No significant differences were detected in baseline characteristics between the two groups. Group 2 patients used renin-angiotensin-aldosterone system blockers (RAASb) less often and more frequently presented with oliguria/anuria. Group 2 patients had significantly lower hemoglobin, serum albumin, and 25-hydroxy-vitamin D (25(OH)D). At the same time, serum phosphate, potassium, and parathyroid hormone (PTH) were significantly higher in Group 2 patients. In a multivariate regression analysis, lack of prior RAASb and lower 25(OH)D levels were independently associated with an increased risk of death or dialysis dependence at discharge. 25(OH)D/PTH ratio was the most accurate predictor of the composite endpoint (Sensitivity: 79.4%, Specificity: 70.4%).

Conclusion: Lack of prior RAASb use, high PTH, low 25(OH)D levels, and low 25(OH) D/PTH ratio are associated with a poor prognosis in patients hospitalized for CRS.

Keywords: cardiorenal syndrome, heart failure, kidney disease, vitamin D, renin-angiotensin-aldosterone system blocker

[1]
Vandenberghe, W.; Gevaert, S.; Kellum, J.A.; Bagshaw, S.M.; Peperstraete, H.; Herck, I.; Decruyenaere, J.; Hoste, E.A.J. Acute kidney injury in cardiorenal syndrome type 1 patients: A systematic review and meta-analysis. Cardiorenal Med., 2016, 6(2), 116-128.
[http://dx.doi.org/10.1159/000442300] [PMID: 26989397]
[2]
Hebert, K.; Dias, A.; Delgado, M.C.; Franco, E.; Tamariz, L.; Steen, D.; Trahan, P.; Major, B.; Arcement, L.M. Epidemiology and survival of the five stages of chronic kidney disease in a systolic heart failure population. Eur. J. Heart Fail., 2010, 12(8), 861-865.
[http://dx.doi.org/10.1093/eurjhf/hfq077] [PMID: 20484366]
[3]
Cheung, A.K.; Sarnak, M.J.; Yan, G.; Berkoben, M.; Heyka, R.; Kaufman, A.; Lewis, J.; Rocco, M.; Toto, R.; Windus, D.; Ornt, D.; Levey, A.S. Cardiac diseases in maintenance hemodialysis patients: Results of the HEMO Study. Kidney Int., 2004, 65(6), 2380-2389.
[http://dx.doi.org/10.1111/j.1523-1755.2004.00657.x] [PMID: 15149351]
[4]
Uduman, J. Epidemiology of cardiorenal syndrome. Adv. Chronic Kidney Dis., 2018, 25(5), 391-399.
[http://dx.doi.org/10.1053/j.ackd.2018.08.009] [PMID: 30309456]
[5]
Zannad, F.; Rossignol, P. Cardiorenal syndrome revisited. Circulation, 2018, 138(9), 929-944.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.117.028814] [PMID: 30354446]
[6]
Theofilis, P.; Vordoni, A.; Koukoulaki, M.; Vlachopanos, G.; Kalaitzidis, R.G. Dyslipidemia in chronic kidney disease: Contemporary concepts and future therapeutic perspectives. Am. J. Nephrol., 2021, 52(9), 693-701.
[http://dx.doi.org/10.1159/000518456] [PMID: 34569479]
[7]
Oikonomou, E.; Leopoulou, M.; Theofilis, P.; Antonopoulos, A.S.; Siasos, G.; Latsios, G.; Mystakidi, V.C.; Antoniades, C.; Tousoulis, D. A link between inflammation and thrombosis in atherosclerotic cardiovascular diseases: Clinical and therapeutic implications. Atherosclerosis, 2020, 309, 16-26.
[http://dx.doi.org/10.1016/j.atherosclerosis.2020.07.027] [PMID: 32858395]
[8]
Sagris, M.; Theofilis, P.; Antonopoulos, A.S.; Oikonomou, E.; Paschaliori, C.; Galiatsatos, N.; Tsioufis, K.; Tousoulis, D. Inflammation in coronary microvascular dysfunction. Int. J. Mol. Sci., 2021, 22(24), 13471.
[http://dx.doi.org/10.3390/ijms222413471] [PMID: 34948272]
[9]
Sagris, M.; Theofilis, P.; Antonopoulos, A.S.; Tsioufis, C.; Oikonomou, E.; Antoniades, C.; Crea, F.; Kaski, J.C.; Tousoulis, D. Inflammatory mechanisms in COVID-19 and atherosclerosis: Current pharmaceutical perspectives. Int. J. Mol. Sci., 2021, 22(12), 6607.
[http://dx.doi.org/10.3390/ijms22126607] [PMID: 34205487]
[10]
Theofilis, P.; Sagris, M.; Oikonomou, E.; Antonopoulos, A.S.; Siasos, G.; Tsioufis, C.; Tousoulis, D. Inflammatory mechanisms contributing to endothelial dysfunction. Biomedicines, 2021, 9(7), 781.
[http://dx.doi.org/10.3390/biomedicines9070781] [PMID: 34356845]
[11]
Delgado-Valero, B.; Cachofeiro, V.; Martínez-Martínez, E. Fibrosis, the bad actor in cardiorenal syndromes: Mechanisms involved. Cells, 2021, 10(7), 1824.
[http://dx.doi.org/10.3390/cells10071824] [PMID: 34359993]
[12]
Rangaswami, J.; Bhalla, V.; Blair, J.E.A.; Chang, T.I.; Costa, S.; Lentine, K.L.; Lerma, E.V.; Mezue, K.; Molitch, M.; Mullens, W.; Ronco, C.; Tang, W.H.W.; McCullough, P.A. Cardiorenal Syndrome: Classification, pathophysiology, diagnosis, and treatment strategies: A scientific statement from the American Heart Association. Circulation, 2019, 139(16), e840-e878.
[http://dx.doi.org/10.1161/CIR.0000000000000664] [PMID: 30852913]
[13]
Ronco, C.; McCullough, P.; Anker, S.D.; Anand, I.; Aspromonte, N.; Bagshaw, S.M.; Bellomo, R.; Berl, T.; Bobek, I.; Cruz, D.N.; Daliento, L.; Davenport, A.; Haapio, M.; Hillege, H.; House, A.A.; Katz, N.; Maisel, A.; Mankad, S.; Zanco, P.; Mebazaa, A.; Palazzuoli, A.; Ronco, F.; Shaw, A.; Sheinfeld, G.; Soni, S.; Vescovo, G.; Zamperetti, N.; Ponikowski, P. Cardio-renal syndromes: Report from the consensus conference of the acute dialysis quality initiative. Eur. Heart J., 2010, 31(6), 703-711.
[http://dx.doi.org/10.1093/eurheartj/ehp507] [PMID: 20037146]
[14]
von Elm, E.; Altman, D.G.; Egger, M.; Pocock, S.J.; Gøtzsche, P.C.; Vandenbroucke, J.P.; Initiative, S. Strengthening the reporting of observational studies in epidemiology (STROBE) statement: Guidelines for reporting observational studies. BMJ, 2007, 335(7624), 806-808.
[http://dx.doi.org/10.1136/bmj.39335.541782.AD] [PMID: 17947786]
[15]
Inker, L.A.; Eneanya, N.D.; Coresh, J.; Tighiouart, H.; Wang, D.; Sang, Y.; Crews, D.C.; Doria, A.; Estrella, M.M.; Froissart, M.; Grams, M.E.; Greene, T.; Grubb, A.; Gudnason, V.; Gutiérrez, O.M.; Kalil, R.; Karger, A.B.; Mauer, M.; Navis, G.; Nelson, R.G.; Poggio, E.D.; Rodby, R.; Rossing, P.; Rule, A.D.; Selvin, E.; Seegmiller, J.C.; Shlipak, M.G.; Torres, V.E.; Yang, W.; Ballew, S.H.; Couture, S.J.; Powe, N.R.; Levey, A.S. New creatinine- and cystatin c-based equations to estimate GFR without race. N. Engl. J. Med., 2021, 385(19), 1737-1749.
[http://dx.doi.org/10.1056/NEJMoa2102953] [PMID: 34554658]
[16]
McDonagh, T.A.; Metra, M.; Adamo, M.; Gardner, R.S.; Baumbach, A.; Böhm, M.; Burri, H.; Butler, J.; Čelutkienė, J.; Chioncel, O.; Cleland, J.G.F.; Coats, A.J.S.; Crespo-Leiro, M.G.; Farmakis, D.; Gilard, M.; Heymans, S.; Hoes, A.W.; Jaarsma, T.; Jankowska, E.A.; Lainscak, M.; Lam, C.S.P.; Lyon, A.R.; McMurray, J.J.V.; Mebazaa, A.; Mindham, R.; Muneretto, C.; Francesco Piepoli, M.; Price, S.; Rosano, G.M.C.; Ruschitzka, F.; Kathrine Skibelund, A.; Group, E.S.C.S.D. 2021 ESC guidelines for the diagnosis and treatment of acute and chronic heart failure. Eur. Heart J., 2021, 42(36), 3599-3726.
[http://dx.doi.org/10.1093/eurheartj/ehab368] [PMID: 34447992]
[17]
Lang, R.M.; Badano, L.P.; Mor-Avi, V.; Afilalo, J.; Armstrong, A.; Ernande, L.; Flachskampf, F.A.; Foster, E.; Goldstein, S.A.; Kuznetsova, T.; Lancellotti, P.; Muraru, D.; Picard, M.H.; Rietzschel, E.R.; Rudski, L.; Spencer, K.T.; Tsang, W.; Voigt, J.U. Recommendations for cardiac chamber quantification by echocardiography in adults: An update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J. Am. Soc. Echocardiogr., 2015, 28(1), 1-39.e14.
[http://dx.doi.org/10.1016/j.echo.2014.10.003] [PMID: 25559473]
[18]
Devereux, R.B.; Alonso, D.R.; Lutas, E.M.; Gottlieb, G.J.; Campo, E.; Sachs, I.; Reichek, N. Echocardiographic assessment of left ventricular hypertrophy: Comparison to necropsy findings. Am. J. Cardiol., 1986, 57(6), 450-458.
[http://dx.doi.org/10.1016/0002-9149(86)90771-X] [PMID: 2936235]
[19]
Nagueh, S.F.; Smiseth, O.A.; Appleton, C.P.; Byrd, B.F., III; Dokainish, H.; Edvardsen, T.; Flachskampf, F.A.; Gillebert, T.C.; Klein, A.L.; Lancellotti, P.; Marino, P.; Oh, J.K.; Popescu, B.A.; Waggoner, A.D. recommendations for the evaluation of left ventricular diastolic function by echocardiography: An update from the American society of echocardiography and the European association of cardiovascular imaging. J. Am. Soc. Echocardiogr., 2016, 29(4), 277-314.
[http://dx.doi.org/10.1016/j.echo.2016.01.011] [PMID: 27037982]
[20]
Augustine, D.X.; Coates-Bradshaw, L.D.; Willis, J.; Harkness, A.; Ring, L.; Grapsa, J.; Coghlan, G.; Kaye, N.; Oxborough, D.; Robinson, S.; Sandoval, J.; Rana, B.S.; Siva, A.; Nihoyannopoulos, P.; Howard, L.S.; Fox, K.; Bhattacharyya, S.; Sharma, V.; Steeds, R.P.; Mathew, T. Echocardiographic assessment of pulmonary hypertension: A guideline protocol from the British Society of Echocardiography. Echo Res. Pract., 2018, 5(3), G11-G24.
[http://dx.doi.org/10.1530/ERP-17-0071] [PMID: 30012832]
[21]
Zoghbi, W.A.; Adams, D.; Bonow, R.O.; Enriquez-Sarano, M.; Foster, E.; Grayburn, P.A.; Hahn, R.T.; Han, Y.; Hung, J.; Lang, R.M.; Little, S.H.; Shah, D.J.; Shernan, S.; Thavendiranathan, P.; Thomas, J.D.; Weissman, N.J. Recommendations for noninvasive evaluation of native valvular regurgitation: a report from the american society of echocardiography developed in collaboration with the society for cardiovascular magnetic resonance. J. Am. Soc. Echocardiogr., 2017, 30(4), 303-371.
[http://dx.doi.org/10.1016/j.echo.2017.01.007] [PMID: 28314623]
[22]
Porter, T.R.; Shillcutt, S.K.; Adams, M.S.; Desjardins, G.; Glas, K.E.; Olson, J.J.; Troughton, R.W. Guidelines for the use of echocardiography as a monitor for therapeutic intervention in adults: A report from the American Society of Echocardiography. J. Am. Soc. Echocardiogr., 2015, 28(1), 40-56.
[http://dx.doi.org/10.1016/j.echo.2014.09.009] [PMID: 25559474]
[23]
Le, N.Q.K.; Hung, T.N.K.; Do, D.T.; Lam, L.H.T.; Dang, L.H.; Huynh, T.T. Radiomics-based machine learning model for efficiently classifying transcriptome subtypes in glioblastoma patients from MRI. Comput. Biol. Med., 2021, 132, 104320.
[http://dx.doi.org/10.1016/j.compbiomed.2021.104320] [PMID: 33735760]
[24]
Do, D.T.; Le, N.Q.K. Using extreme gradient boosting to identify origin of replication in Saccharomyces cerevisiae via hybrid features. Genomics, 2020, 112(3), 2445-2451.
[http://dx.doi.org/10.1016/j.ygeno.2020.01.017] [PMID: 31987913]
[25]
Fluss, R.; Faraggi, D.; Reiser, B. Estimation of the Youden Index and its associated cutoff point. Biom. J., 2005, 47(4), 458-472.
[http://dx.doi.org/10.1002/bimj.200410135] [PMID: 16161804]
[26]
Fu, S.; Zhao, S.; Ye, P.; Luo, L. Biomarkers in cardiorenal syndromes. BioMed Res. Int., 2018, 2018, 9617363.
[http://dx.doi.org/10.1155/2018/9617363] [PMID: 29693019]
[27]
Pascual-Figal, D.A.; Caballero, L.; Sanchez-Mas, J.; Lax, A. Prognostic markers for acute heart failure. Expert Opin. Med. Diagn., 2013, 7(4), 379-392.
[http://dx.doi.org/10.1517/17530059.2013.814638] [PMID: 23795649]
[28]
Metra, M.; Cotter, G.; El-Khorazaty, J.; Davison, B.A.; Milo, O.; Carubelli, V.; Bourge, R.C.; Cleland, J.G.; Jondeau, G.; Krum, H.; O’Connor, C.M.; Parker, J.D.; Torre-Amione, G.; van Veldhuisen, D.J.; Rainisio, M.; Kobrin, I.; McMurray, J.J.; Teerlink, J.R. Acute heart failure in the elderly: Differences in clinical characteristics, outcomes, and prognostic factors in the VERITAS Study. J. Card. Fail., 2015, 21(3), 179-188.
[http://dx.doi.org/10.1016/j.cardfail.2014.12.012] [PMID: 25573829]
[29]
Huang, G.; Qin, J.; Deng, X.; Luo, G.; Yu, D.; Zhang, M.; Zhou, S.; Wang, L. Prognostic value of serum uric acid in patients with acute heart failure: A meta-analysis. Medicine (Baltimore), 2019, 98(8), e14525.
[http://dx.doi.org/10.1097/MD.0000000000014525] [PMID: 30813158]
[30]
Ruiz-Hurtado, G.; Ruilope, L.M. Cardiorenal protection during chronic renin-angiotensin-aldosterone system suppression: Evidences and caveats. Eur. Heart J. Cardiovasc. Pharmacother., 2015, 1(2), 126-131.
[http://dx.doi.org/10.1093/ehjcvp/pvu023] [PMID: 27533982]
[31]
Kidney disease: Improving global outcomes (KDIGO) blood pressure work group. KDIGO 2021 clinical practice guideline for the management of blood pressure in chronic kidney disease. Kidney Int., 2021, 99(3S), S1-S87.
[PMID: 33637192]
[32]
Kidney disease: Improving global outcomes (KDIGO) diabetes work group. KDIGO 2020 Clinical Practice Guideline for Diabetes Management in Chronic Kidney Disease. Kidney Int., 2020, 98(4S), S1-S115.
[PMID: 32998798]
[33]
Yildirim, T.; Arici, M.; Piskinpasa, S.; Aybal-Kutlugun, A.; Yilmaz, R.; Altun, B.; Erdem, Y.; Turgan, C. Major barriers against renin-angiotensin-aldosterone system blocker use in chronic kidney disease stages 3-5 in clinical practice: A safety concern? Ren. Fail., 2012, 34(9), 1095-1099.
[http://dx.doi.org/10.3109/0886022X.2012.717478] [PMID: 22950572]
[34]
Humphrey, T.J.L.; James, G.; Wittbrodt, E.T.; Zarzuela, D.; Hiemstra, T.F. Adverse clinical outcomes associated with RAAS inhibitor discontinuation: Analysis of over 400 000 patients from the UK Clinical Practice Research Datalink (CPRD). Clin. Kidney J., 2021, 14(10), 2203-2212.
[http://dx.doi.org/10.1093/ckj/sfab029] [PMID: 34804520]
[35]
Palmer, B.F. Potassium binders for hyperkalemia in chronic kidney disease-diet, renin-angiotensin-aldosterone system inhibitor therapy, and hemodialysis. Mayo Clin. Proc., 2020, 95(2), 339-354.
[http://dx.doi.org/10.1016/j.mayocp.2019.05.019] [PMID: 31668450]
[36]
Silva-Cardoso, J.; Brito, D.; Frazão, J.M.; Ferreira, A.; Bettencourt, P.; Branco, P.; Fonseca, C. Management of RAASi-associated hyperkalemia in patients with cardiovascular disease. Heart Fail. Rev., 2021, 26(4), 891-896.
[http://dx.doi.org/10.1007/s10741-020-10069-3] [PMID: 33599908]
[37]
Ahmed, A.K.; Kamath, N.S.; El Kossi, M.; El Nahas, A.M. The impact of stopping inhibitors of the renin-angiotensin system in patients with advanced chronic kidney disease. Nephrol. Dial. Transplant., 2010, 25(12), 3977-3982.
[http://dx.doi.org/10.1093/ndt/gfp511] [PMID: 19820248]
[38]
Qiao, Y.; Shin, J-I.; Chen, T.K.; Inker, L.A.; Coresh, J.; Alexander, G.C.; Jackson, J.W.; Chang, A.R.; Grams, M.E. Association between renin-angiotensin system blockade discontinuation and all-cause mortality among persons with low estimated glomerular filtration rate. JAMA Intern. Med., 2020, 180(5), 718-726.
[http://dx.doi.org/10.1001/jamainternmed.2020.0193] [PMID: 32150237]
[39]
Panteli, A.E.; Theofilis, P.; Vordoni, A.; Vlachopanos, G.; Koukoulaki, M.; Kalaitzidis, R.G. Narrative review of recent studies on the role of vitamin D in the prevention of cardiac and renal risk and additional considerations for COVID-19 vulnerability. Curr. Vasc. Pharmacol., 2021. [Epub ahead of print].
[http://dx.doi.org/10.2174/1570161119666211119142746] [PMID: 34802405]
[40]
Zapatero, A.; Dot, I.; Diaz, Y.; Gracia, M.P.; Pérez-Terán, P.; Climent, C.; Masclans, J.R.; Nolla, J. Severe vitamin D deficiency upon admission in critically ill patients is related to acute kidney injury and a poor prognosis. Med. Intensiva, 2018, 42(4), 216-224.
[http://dx.doi.org/10.1016/j.medine.2017.07.002] [PMID: 28847615]
[41]
Graidis, S.; Papavramidis, T.S.; Papaioannou, M. Vitamin D and acute kidney injury: A Two-way causality relation and a predictive, prognostic, and therapeutic role of Vitamin D. Front. Nutr., 2021, 7, 630951-630951.
[http://dx.doi.org/10.3389/fnut.2020.630951] [PMID: 33748167]
[42]
Jayedi, A.; Soltani, S.; Shab-Bidar, S.; Vitamin, D. Vitamin D status and all-cause mortality in patients with chronic kidney disease: A systematic review and dose-response meta-analysis. J. Clin. Endocrinol. Metab., 2017, 102(7), 2136-2145.
[http://dx.doi.org/10.1210/jc.2017-00105] [PMID: 28453636]
[43]
Dai, L.; Liu, M.; Chen, L. Association of Serum 25-Hydroxyvitamin D concentrations with all-cause and cause-specific mortality among adult patients with existing cardiovascular disease. Front. Nutr., 2021, 8(693), 740855.
[http://dx.doi.org/10.3389/fnut.2021.740855] [PMID: 34631770]
[44]
Cubbon, R.M.; Lowry, J.E.; Drozd, M.; Hall, M.; Gierula, J.; Paton, M.F.; Byrom, R.; Kearney, L.C.; Barth, J.H.; Kearney, M.T.; Witte, K.K. Vitamin D deficiency is an independent predictor of mortality in patients with chronic heart failure. Eur. J. Nutr., 2019, 58(6), 2535-2543.
[http://dx.doi.org/10.1007/s00394-018-1806-y] [PMID: 30121806]
[45]
Kusunose, K.; Okushi, Y.; Okayama, Y.; Zheng, R.; Abe, M.; Nakai, M.; Sumita, Y.; Ise, T.; Tobiume, T.; Yamaguchi, K.; Yagi, S.; Fukuda, D.; Yamada, H.; Soeki, T.; Wakatsuki, T.; Sata, M. Association between vitamin D and heart failure mortality in 10,974 hospitalized individuals. Nutrients, 2021, 13(2), 335.
[http://dx.doi.org/10.3390/nu13020335] [PMID: 33498709]
[46]
Masson, S.; Barlera, S.; Colotta, F.; Magnoli, M.; Bonelli, F.; Moro, M.; Marchioli, R.; Tavazzi, L.; Tognoni, G.; Latini, R. A low plasma 1,25(OH)2 vitamin D/PTH (1-84) ratio predicts worsening of renal function in patients with chronic heart failure. Int. J. Cardiol., 2016, 224, 220-225.
[http://dx.doi.org/10.1016/j.ijcard.2016.09.014] [PMID: 27657477]
[47]
Siasos, G.; Theofilis, P.; Oikonomou, E.; Tousoulis, D.; Vitamin, D. Vitamin D: A cardiovascular risk biomarker or a treatment target? Hellenic J. Cardiol., 2019, 60(2), 114-116.
[http://dx.doi.org/10.1016/j.hjc.2019.03.011] [PMID: 31271779]
[48]
Lu, R.J.; Zhu, S.M.; Tang, F.L.; Zhu, X.S.; Fan, Z.D.; Wang, G.L.; Jiang, Y.F.; Zhang, Y. Effects of vitamin D or its analogues on the mortality of patients with chronic kidney disease: An updated systematic review and meta-analysis. Eur. J. Clin. Nutr., 2017, 71(6), 683-693.
[http://dx.doi.org/10.1038/ejcn.2017.59] [PMID: 28488689]
[49]
Zhao, J.D.; Jia, J.J.; Dong, P.S.; Zhao, D.; Yang, X.M.; Li, D.L.; Zhang, H.F. Effect of vitamin D on ventricular remodelling in heart failure: A meta-analysis of randomised controlled trials. BMJ Open, 2018, 8(8), e020545.
[http://dx.doi.org/10.1136/bmjopen-2017-020545] [PMID: 30166289]
[50]
Boucher, B.J. Why do so many trials of vitamin D supplementation fail? Endocr. Connect., 2020, 9(9), R195-R206.
[http://dx.doi.org/10.1530/EC-20-0274] [PMID: 33052876]
[51]
Sempos, C.T.; Durazo-Arvizu, R.A.; Dawson-Hughes, B.; Yetley, E.A.; Looker, A.C.; Schleicher, R.L.; Cao, G.; Burt, V.; Kramer, H.; Bailey, R.L.; Dwyer, J.T.; Zhang, X.; Gahche, J.; Coates, P.M.; Picciano, M.F. Is there a reverse J-shaped association between 25-hydroxyvitamin D and all-cause mortality? Results from the U.S. nationally representative NHANES. J. Clin. Endocrinol. Metab., 2013, 98(7), 3001-3009.
[http://dx.doi.org/10.1210/jc.2013-1333] [PMID: 23666975]
[52]
Scicchitano, P.; Massari, F. Bioimpedance vector analysis in the evaluation of congestion in heart failure. Biomarkers Med., 2020, 14(2), 81-85.
[http://dx.doi.org/10.2217/bmm-2019-0429] [PMID: 32053026]
[53]
Massari, F.; Scicchitano, P.; Ciccone, M.M.; Caldarola, P.; Aspromonte, N.; Iacoviello, M.; Barro, S.; Pantano, I.; Valle, R. Bioimpedance vector analysis predicts hospital length of stay in acute heart failure. Nutrition, 2019, 61, 56-60.
[http://dx.doi.org/10.1016/j.nut.2018.10.028] [PMID: 30703569]