Evidence that tirzepatide protects against diabetes-related cardiac damages.

AC16 cell line GIP receptor GLP-1 receptor. Heart failure High glucose Tirzepatide

Journal

Cardiovascular diabetology
ISSN: 1475-2840
Titre abrégé: Cardiovasc Diabetol
Pays: England
ID NLM: 101147637

Informations de publication

Date de publication:
30 Mar 2024
Historique:
received: 06 02 2024
accepted: 14 03 2024
medline: 31 3 2024
pubmed: 31 3 2024
entrez: 30 3 2024
Statut: epublish

Résumé

Glucagon-like peptide-1 receptor agonists (GLP-1RAs) are effective antidiabetic drugs with potential cardiovascular benefits. Despite their well-established role in reducing the risk of major adverse cardiovascular events (MACE), their impact on heart failure (HF) remains unclear. Therefore, our study examined the cardioprotective effects of tirzepatide (TZT), a novel glucose-dependent insulinotropic polypeptide (GIP) and glucagon-like peptide 1 (GLP-1) receptor agonist. A three-steps approach was designed: (i) Meta-analysis investigation with the primary objective of assessing major adverse cardiovascular events (MACE) occurrence from major randomized clinical trials.; (ii) TZT effects on a human cardiac AC16 cell line exposed to normal (5 mM) and high (33 mM) glucose concentrations for 7 days. The gene expression and protein levels of primary markers related to cardiac fibrosis, hypertrophy, and calcium modulation were evaluated. (iii) In silico data from bioinformatic analyses for generating an interaction map that delineates the potential mechanism of action of TZT. Meta-analysis showed a reduced risk for MACE events by TZT therapy (HR was 0.59 (95% CI 0.40-0.79, Heterogeneity: r Our findings indicate that TZT has beneficial effects on cardiac cells by positively modulating cardiomyocyte death, fibrosis, and hypertrophy in the presence of high glucose concentrations. This suggests that TZT may reduce the risk of diabetes-related cardiac damage, highlighting its potential as a therapeutic option for heart failure management clinical trials. Our study strongly supports the rationale behind the clinical trials currently underway, the results of which will be further investigated to gain insights into the cardiovascular safety and efficacy of TZT.

Sections du résumé

BACKGROUND BACKGROUND
Glucagon-like peptide-1 receptor agonists (GLP-1RAs) are effective antidiabetic drugs with potential cardiovascular benefits. Despite their well-established role in reducing the risk of major adverse cardiovascular events (MACE), their impact on heart failure (HF) remains unclear. Therefore, our study examined the cardioprotective effects of tirzepatide (TZT), a novel glucose-dependent insulinotropic polypeptide (GIP) and glucagon-like peptide 1 (GLP-1) receptor agonist.
METHODS METHODS
A three-steps approach was designed: (i) Meta-analysis investigation with the primary objective of assessing major adverse cardiovascular events (MACE) occurrence from major randomized clinical trials.; (ii) TZT effects on a human cardiac AC16 cell line exposed to normal (5 mM) and high (33 mM) glucose concentrations for 7 days. The gene expression and protein levels of primary markers related to cardiac fibrosis, hypertrophy, and calcium modulation were evaluated. (iii) In silico data from bioinformatic analyses for generating an interaction map that delineates the potential mechanism of action of TZT.
RESULTS RESULTS
Meta-analysis showed a reduced risk for MACE events by TZT therapy (HR was 0.59 (95% CI 0.40-0.79, Heterogeneity: r
CONCLUSION CONCLUSIONS
Our findings indicate that TZT has beneficial effects on cardiac cells by positively modulating cardiomyocyte death, fibrosis, and hypertrophy in the presence of high glucose concentrations. This suggests that TZT may reduce the risk of diabetes-related cardiac damage, highlighting its potential as a therapeutic option for heart failure management clinical trials. Our study strongly supports the rationale behind the clinical trials currently underway, the results of which will be further investigated to gain insights into the cardiovascular safety and efficacy of TZT.

Identifiants

pubmed: 38555463
doi: 10.1186/s12933-024-02203-4
pii: 10.1186/s12933-024-02203-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

112

Subventions

Organisme : PROGETTI DI RICERCA DI RILEVANTE INTERESSE NAZIONALE - Bando 2020
ID : 2020N5WK98
Organisme : AdvaNced Technologies for Human-centrEd Medicine (project acronym: ANTHEM
ID : PNC0000003
Organisme : PRIN: PROGETTI DI RICERCA DI RILEVANTE INTERESSE NAZIONALE / Bando 2022
ID : 2022CX7HTJ

Informations de copyright

© 2024. The Author(s).

Références

Marso SP, Daniels GH, Brown-Frandsen K, Kristensen P, Mann JF, Nauck MA, Nissen SE, Pocock S, Poulter NR, Ravn LS, et al. Liraglutide and cardiovascular outcomes in type 2 diabetes. N Engl J Med. 2016;375(4):311–22.
pubmed: 27295427 pmcid: 4985288 doi: 10.1056/NEJMoa1603827
Marso SP, Bain SC, Consoli A, Eliaschewitz FG, Jodar E, Leiter LA, Lingvay I, Rosenstock J, Seufert J, Warren ML, et al. Semaglutide and cardiovascular outcomes in patients with type 2 diabetes. N Engl J Med. 2016;375(19):1834–44.
pubmed: 27633186 doi: 10.1056/NEJMoa1607141
Gerstein HC, Colhoun HM, Dagenais GR, Diaz R, Lakshmanan M, Pais P, Probstfield J, Riesmeyer JS, Riddle MC, Ryden L, et al. Dulaglutide and cardiovascular outcomes in type 2 diabetes (REWIND): a double-blind, randomised placebo-controlled trial. Lancet. 2019;394(10193):121–30.
pubmed: 31189511 doi: 10.1016/S0140-6736(19)31149-3
Piccini S, Favacchio G, Panico C, Morenghi E, Folli F, Mazziotti G, Lania AG, Mirani M. Time-dependent effect of GLP-1 receptor agonists on cardiovascular benefits: a real-world study. Cardiovasc Diabetol. 2023;22(1):69.
pubmed: 36966321 pmcid: 10039680 doi: 10.1186/s12933-023-01800-z
Marfella R, Nappo F, De Angelis L, Paolisso G, Tagliamonte MR, Giugliano D. Hemodynamic effects of acute hyperglycemia in type 2 diabetic patients. Diabetes Care. 2000;23(5):658–63.
pubmed: 10834426 doi: 10.2337/diacare.23.5.658
Sardu C, Consiglia Trotta M, Santella B, D’Onofrio N, Barbieri M, Rizzo MR, Sasso FC, Scisciola L, Turriziani F, Torella M, et al. Microbiota thrombus colonization may influence athero-thrombosis in hyperglycemic patients with ST segment elevation myocardialinfarction (STEMI) Marianella study. Diabetes Res Clin Pract. 2021;173: 108670.
pubmed: 33453294 doi: 10.1016/j.diabres.2021.108670
Monzo L, Ferrari I, Cicogna F, Tota C, Cice G, Girerd N, Calo L. Sodium-glucose co-transporter 2 inhibitors in heart failure: an updated evidence-based practical guidance for clinicians. Eur Heart J Suppl. 2023;25(Suppl C):C309–15.
pubmed: 37125324 pmcid: 10132577 doi: 10.1093/eurheartjsupp/suad055
Kreiner FF, Hovingh GKK, von Scholten BJ. The potential of glucagon-like peptide-1 receptor agonists in heart failure. Front Physiol. 2022;13: 983961.
pubmed: 36203939 pmcid: 9531309 doi: 10.3389/fphys.2022.983961
Ma X, Liu Z, Ilyas I, Little PJ, Kamato D, Sahebka A, Chen Z, Luo S, Zheng X, Weng J, et al. GLP-1 receptor agonists (GLP-1RAs): cardiovascular actions and therapeutic potential. Int J Biol Sci. 2021;17(8):2050–68.
pubmed: 34131405 pmcid: 8193264 doi: 10.7150/ijbs.59965
Baggio LL, Yusta B, Mulvihill EE, Cao X, Streutker CJ, Butany J, Cappola TP, Margulies KB, Drucker DJ. GLP-1 Receptor expression within the human heart. Endocrinology. 2018;159(4):1570–84.
pubmed: 29444223 pmcid: 5939638 doi: 10.1210/en.2018-00004
Nreu B, Dicembrini I, Tinti F, Sesti G, Mannucci E, Monami M. Major cardiovascular events, heart failure, and atrial fibrillation in patients treated with glucagon-like peptide-1 receptor agonists: an updated meta-analysis of randomized controlled trials. Nutr Metab Cardiovasc Dis. 2020;30(7):1106–14.
pubmed: 32448716 doi: 10.1016/j.numecd.2020.03.013
Song R, Qian H, Wang Y, Li Q, Li D, Chen J, Yang J, Zhong J, Yang H, Min X, et al. Research progress on the cardiovascular protective effect of glucagon-like peptide-1 receptor agonists. J Diabetes Res. 2022;2022:4554996.
pubmed: 35434139 pmcid: 9012640 doi: 10.1155/2022/4554996
Fisman EZ, Tenenbaum A. The dual glucose-dependent insulinotropic polypeptide (GIP) and glucagon-like peptide-1 (GLP-1) receptor agonist tirzepatide: a novel cardiometabolic therapeutic prospect. Cardiovasc Diabetol. 2021;20(1):225.
pubmed: 34819089 pmcid: 8613929 doi: 10.1186/s12933-021-01412-5
Dutta P, Kumar Y, Babu AT, Giri Ravindran S, Salam A, Rai B, Baskar A, Dhawan A, Jomy M. Tirzepatide: a promising drug for type 2 diabetes and beyond. Cureus. 2023;15(5): e38379.
pubmed: 37265914 pmcid: 10231274
Cho YK, La Lee Y, Jung CH. The cardiovascular effect of tirzepatide: a glucagon-like peptide-1 and glucose-dependent insulinotropic polypeptide dual agonist. J Lipid Atheroscler. 2023;12(3):213–22.
pubmed: 37800107 pmcid: 10548186 doi: 10.12997/jla.2023.12.3.213
Nicholls SJ, Bhatt DL, Buse JB, Prato SD, Kahn SE, Lincoff AM, McGuire DK, Nauck MA, Nissen SE, Sattar N, et al. Comparison of tirzepatide and dulaglutide on major adverse cardiovascular events in participants with type 2 diabetes and atherosclerotic cardiovascular disease: SURPASS-CVOT design and baseline characteristics. Am Heart J. 2023;267:1–11.
pubmed: 37758044 doi: 10.1016/j.ahj.2023.09.007
Del Prato S, Kahn SE, Pavo I, Weerakkody GJ, Yang Z, Doupis J, Aizenberg D, Wynne AG, Riesmeyer JS, Heine RJ, et al. Tirzepatide versus insulin glargine in type 2 diabetes and increased cardiovascular risk (SURPASS-4): a randomised, open-label, parallel-group, multicentre, phase 3 trial. Lancet. 2021;398(10313):1811–24.
pubmed: 34672967 doi: 10.1016/S0140-6736(21)02188-7
Patoulias D, Papadopoulos C, Fragakis N, Doumas M. Updated meta-analysis assessing the cardiovascular efficacy of tirzepatide. Am J Cardiol. 2022;181:139–40.
pubmed: 35977865 doi: 10.1016/j.amjcard.2022.07.003
Marfella R, Scisciola L, D’Onofrio N, Maiello C, Trotta MC, Sardu C, Panarese I, Ferraraccio F, Capuano A, Barbieri M, et al. Sodium-glucose cotransporter-2 (SGLT2) expression in diabetic and non-diabetic failing human cardiomyocytes. Pharmacol Res. 2022;184: 106448.
pubmed: 36096423 doi: 10.1016/j.phrs.2022.106448
Kenny HC, Abel ED. Heart failure in type 2 diabetes mellitus. Circ Res. 2019;124(1):121–41.
pubmed: 30605420 pmcid: 6447311 doi: 10.1161/CIRCRESAHA.118.311371
Perez-Belmonte LM, Sanz-Canovas J, Garcia de Lucas MD, Ricci M, Aviles-Bueno B, Cobos-Palacios L, Perez-Velasco MA, Lopez-Sampalo A, Bernal-Lopez MR, Jansen-Chaparro S, et al. Efficacy and safety of semaglutide for the management of obese patients with type 2 diabetes and chronic heart failure in real-world clinical practice. Front Endocrinol. 2022;13:851035.
doi: 10.3389/fendo.2022.851035
Withaar C, Meems LMG, Markousis-Mavrogenis G, Boogerd CJ, Sillje HHW, Schouten EM, Dokter MM, Voors AA, Westenbrink BD, Lam CSP, et al. The effects of liraglutide and dapagliflozin on cardiac function and structure in a multi-hit mouse model of heart failure with preserved ejection fraction. Cardiovasc Res. 2021;117(9):2108–24.
pubmed: 32871009 doi: 10.1093/cvr/cvaa256
Huixing L, Di F, Daoquan P. Effect of glucagon-like peptide-1 receptor agonists on prognosis of heart failure and cardiac function: a systematic review and meta-analysis of randomized controlled trials. Clin Ther. 2023;45(1):17–30.
pubmed: 36604209 doi: 10.1016/j.clinthera.2022.12.006
Neves JS, Packer M, Ferreira JP. Increased risk of heart failure hospitalization with GLP-1 receptor agonists in patients with reduced ejection fraction: a meta-analysis of the EXSCEL and fight trials. J Card Fail. 2023;29(7):1107–9.
pubmed: 37028749 doi: 10.1016/j.cardfail.2023.03.017
Sardu C, Barbieri M, Rizzo MR, Paolisso P, Paolisso G, Marfella R. Cardiac resynchronization therapy outcomes in type 2 diabetic patients: role of MicroRNA changes. J Diabetes Res. 2016;2016:7292564.
pubmed: 26636106 doi: 10.1155/2016/7292564
D’Onofrio N, Sardu C, Paolisso P, Minicucci F, Gragnano F, Ferraraccio F, Panarese I, Scisciola L, Mauro C, Rizzo MR, et al. MicroRNA-33 and SIRT1 influence the coronary thrombus burden in hyperglycemic STEMI patients. J Cell Physiol. 2020;235(2):1438–52.
pubmed: 31294459 doi: 10.1002/jcp.29064
Farzam K, Patel P. Tirzepatide. Treasure Island. 2023;24(3):10449.
Pirro V, Roth KD, Lin Y, Willency JA, Milligan PL, Wilson JM, Ruotolo G, Haupt A, Newgard CB, Duffin KL. Effects of tirzepatide, a dual GIP and GLP-1 RA, on lipid and metabolite profiles in subjects with type 2 diabetes. J Clin Endocrinol Metab. 2022;107(2):363–78.
pubmed: 34608929 doi: 10.1210/clinem/dgab722
Ussher JR, Baggio LL, Campbell JE, Mulvihill EE, Kim M, Kabir MG, Cao X, Baranek BM, Stoffers DA, Seeley RJ, et al. Inactivation of the cardiomyocyte glucagon-like peptide-1 receptor (GLP-1R) unmasks cardiomyocyte-independent GLP-1R-mediated cardioprotection. Mol Metab. 2014;3(5):507–17.
pubmed: 25061556 pmcid: 4099509 doi: 10.1016/j.molmet.2014.04.009
Willard FS, Douros JD, Gabe MB, Showalter AD, Wainscott DB, Suter TM, Capozzi ME, van der Velden WJ, Stutsman C, Cardona GR, et al. Tirzepatide is an imbalanced and biased dual GIP and GLP-1 receptor agonist. JCI Insight. 2020. https://doi.org/10.1172/jci.insight.140532 .
doi: 10.1172/jci.insight.140532 pubmed: 32730231 pmcid: 7526454
Frias JP, Nauck MA, Van J, Kutner ME, Cui X, Benson C, Urva S, Gimeno RE, Milicevic Z, Robins D, et al. Efficacy and safety of LY3298176, a novel dual GIP and GLP-1 receptor agonist, in patients with type 2 diabetes: a randomised, placebo-controlled and active comparator-controlled phase 2 trial. Lancet. 2018;392(10160):2180–93.
pubmed: 30293770 doi: 10.1016/S0140-6736(18)32260-8
Liu Q, Zhu J, Kong B, Shuai W, Huang H. Tirzepatide attenuates lipopolysaccharide-induced left ventricular remodeling and dysfunction by inhibiting the TLR4/NF-kB/NLRP3 pathway. Int Immunopharmacol. 2023;120: 110311.
pubmed: 37196559 doi: 10.1016/j.intimp.2023.110311
Becirovic-Agic M, Chalise U, Daseke MJ, Konfrst S, Salomon JD, Mishra PK, Lindsey ML. Infarct in the heart: what’s MMP-9 got to do with It? Biomolecules. 2021;11(4):491.
pubmed: 33805901 pmcid: 8064345 doi: 10.3390/biom11040491
Aguirre F, Abrigo J, Gonzalez F, Gonzalez A, Simon F, Cabello-Verrugio C. Protective effect of angiotensin 1–7 on sarcopenia induced by chronic liver disease in mice. Int J Mol Sci. 2020;21(11):3891.
pubmed: 32485991 pmcid: 7312494 doi: 10.3390/ijms21113891
Wu X, Qian L, Zhao H, Lei W, Liu Y, Xu X, Li J, Yang Z, Wang D, Zhang Y, et al. CXCL12/CXCR4: an amazing challenge and opportunity in the fight against fibrosis. Ageing Res Rev. 2023;83: 101809.
pubmed: 36442720 doi: 10.1016/j.arr.2022.101809
Li R, Shan Y, Gao L, Wang X, Wang X, Wang F. The Glp-1 analog liraglutide protects against angiotensin ii and pressure overload-induced cardiac hypertrophy via PI3K/Akt1 and AMPKa signaling. Front Pharmacol. 2019;10:537.
pubmed: 31231210 pmcid: 6560159 doi: 10.3389/fphar.2019.00537
Zhang LH, Pang XF, Bai F, Wang NP, Shah AI, McKallip RJ, Li XW, Wang X, Zhao ZQ. Preservation of glucagon-like peptide-1 level attenuates angiotensin II-induced tissue fibrosis by altering AT1/AT 2 receptor expression and angiotensin-converting enzyme 2 activity in rat heart. Cardiovasc Drugs Ther. 2015;29(3):243–55.
pubmed: 25994830 doi: 10.1007/s10557-015-6592-7
Al-Hassnan ZN, Shinwari ZM, Wakil SM, Tulbah S, Mohammed S, Rahbeeni Z, Alghamdi M, Rababh M, Colak D, Kaya N, et al. A substitution mutation in cardiac ubiquitin ligase, FBXO32, is associated with an autosomal recessive form of dilated cardiomyopathy. BMC Med Genet. 2016;17:3.
pubmed: 26768247 pmcid: 4714499 doi: 10.1186/s12881-016-0267-5
Wu J, Ding P, Wu H, Yang P, Guo H, Tian Y, Meng L, Zhao Q. Sarcopenia: molecular regulatory network for loss of muscle mass and function. Front Nutr. 2023;10:1037200.
pubmed: 36819699 pmcid: 9932270 doi: 10.3389/fnut.2023.1037200
Mankhong S, Kim S, Moon S, Kwak HB, Park DH, Kang JH. Experimental models of sarcopenia: bridging molecular mechanism and therapeutic strategy. Cells. 2020. https://doi.org/10.3390/cells9061385 .
doi: 10.3390/cells9061385 pubmed: 32498474 pmcid: 7348939
Peris-Moreno D, Taillandier D, Polge C. MuRF1/TRIM63 master regulator of muscle mass. Int J Mol Sci. 2020;21(18):6663.
pubmed: 32933049 pmcid: 7555135 doi: 10.3390/ijms21186663
Bodine SC, Baehr LM. Skeletal muscle atrophy and the E3 ubiquitin ligases MuRF1 and MAFbx/atrogin-1. Am J Physiol Endocrinol Metab. 2014;307(6):E469-484.
pubmed: 25096180 pmcid: 4166716 doi: 10.1152/ajpendo.00204.2014
Lee D, Goldberg A. Atrogin1/MAFbx: what atrophy, hypertrophy, and cardiac failure have in common. Circ Res. 2011;109(2):123–6.
pubmed: 21737813 doi: 10.1161/CIRCRESAHA.111.248872
Haberecht-Muller S, Kruger E, Fielitz J. Out of control: the role of the ubiquitin proteasome system in skeletal muscle during inflammation. Biomolecules. 2021. https://doi.org/10.3390/biom11091327 .
doi: 10.3390/biom11091327 pubmed: 34572540 pmcid: 8468834
Mota R, Parry TL, Yates CC, Qiang Z, Eaton SC, Mwiza JM, Tulasi D, Schisler JC, Patterson C, Zaglia T, et al. Increasing cardiomyocyte atrogin-1 reduces aging-associated fibrosis and regulates remodeling in vivo. Am J Pathol. 2018;188(7):1676–92.
pubmed: 29758183 pmcid: 6026801 doi: 10.1016/j.ajpath.2018.04.007
Du F, Cao Y, Ran Y, Wu Q, Chen B. Metformin attenuates angiotensin II-induced cardiomyocyte hypertrophy by upregulating the MuRF1 and MAFbx pathway. Exp Ther Med. 2021;22(5):1231.
pubmed: 34539827 pmcid: 8438677 doi: 10.3892/etm.2021.10665
Nuamnaichati N, Mangmool S, Chattipakorn N, Parichatikanond W. Stimulation of GLP-1 receptor inhibits methylglyoxal-induced mitochondrial dysfunctions in H9c2 cardiomyoblasts: potential role of Epac/PI3K/Akt pathway. Front Pharmacol. 2020;11:805.
pubmed: 32547400 pmcid: 7274035 doi: 10.3389/fphar.2020.00805
Bertaud A, Joshkon A, Heim X, Bachelier R, Bardin N, Leroyer AS, Blot-Chabaud M. signaling pathways and potential therapeutic strategies in cardiac fibrosis. Int J Mol Sci. 2023. https://doi.org/10.3390/ijms24021756 .
doi: 10.3390/ijms24021756 pubmed: 36675283 pmcid: 9866199
Zhang X, Wang Q, Wang Z, Zhang H, Zhu F, Ma J, Wang W, Chen Z, Wang H. Interaction between A-kinase anchoring protein 5 and protein kinase A mediates CaMKII/HDAC signaling to inhibit cardiomyocyte hypertrophy after hypoxic reoxygenation. Cell Signal. 2023;103: 110569.
pubmed: 36565899 doi: 10.1016/j.cellsig.2022.110569
Zhang T, Zhang Y, Cui M, Jin L, Wang Y, Lv F, Liu Y, Zheng W, Shang H, Zhang J, et al. CaMKII is a RIP3 substrate mediating ischemia- and oxidative stress-induced myocardial necroptosis. Nat Med. 2016;22(2):175–82.
pubmed: 26726877 doi: 10.1038/nm.4017
Kreusser MM, Lehmann LH, Keranov S, Hoting MO, Oehl U, Kohlhaas M, Reil JC, Neumann K, Schneider MD, Hill JA, et al. Cardiac CaM Kinase II genes delta and gamma contribute to adverse remodeling but redundantly inhibit calcineurin-induced myocardial hypertrophy. Circulation. 2014;130(15):1262–73.
pubmed: 25124496 pmcid: 4316667 doi: 10.1161/CIRCULATIONAHA.114.006185
Younce CW, Burmeister MA, Ayala JE. Exendin-4 attenuates high glucose-induced cardiomyocyte apoptosis via inhibition of endoplasmic reticulum stress and activation of SERCA2a. Am J Physiol Cell Physiol. 2013;304(6):C508-518.
pubmed: 23302777 doi: 10.1152/ajpcell.00248.2012
Chen J, Wang D, Wang F, Shi S, Chen Y, Yang B, Tang Y, Huang C. Exendin-4 inhibits structural remodeling and improves Ca(2+) homeostasis in rats with heart failure via the GLP-1 receptor through the eNOS/cGMP/PKG pathway. Peptides. 2017;90:69–77.
pubmed: 28242257 doi: 10.1016/j.peptides.2017.02.008

Auteurs

Fatemeh Taktaz (F)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy.

Lucia Scisciola (L)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy. lucia.scisciola@unicampania.it.

Rosaria Anna Fontanella (RA)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy.

Ada Pesapane (A)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy.

Puja Ghosh (P)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy.

Martina Franzese (M)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy.

Giovanni Tortorella (G)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy.

Armando Puocci (A)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy.

Eduardo Sommella (E)

Department of Pharmacy, University of Salerno, Fisciano, SA, Italy.

Giuseppe Signoriello (G)

Department of Mental Health and Public Medicine, Section of Statistic, University of Campania, Naples, Italy.

Fabiola Olivieri (F)

Department of Clinical and Molecular Sciences, DISCLIMO, Università Politecnica delle Marche, Ancona, Italy.
Center of Clinical Pathology and Innovative Therapy, IRCCS INRCA, Ancona, Italy.

Michelangela Barbieri (M)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy.

Giuseppe Paolisso (G)

Department of Advanced Medical and Surgical Sciences, University of Campania ''Luigi Vanvitelli'', P.zza L. Miraglia, 2, 80138, Naples, Italy.
UniCamillus, International Medical University, Rome, Italy.

Classifications MeSH