Download PDF
Homeopathy 2024; 113(02): 098-111
DOI: 10.1055/s-0043-1771024
Original Research Article

Homeopathic Formulations of Syzygium jambolanum Alleviate Glycation-Mediated Structural and Functional Modifications of Albumin: Evaluation through Multi-Spectroscopic and Microscopic Approaches

Nilima S. Bangar
1   Symbiosis School of Biological Sciences, Symbiosis International (Deemed University), Lavale, Pune, Maharashtra, India
,
Selvan Ravindran
1   Symbiosis School of Biological Sciences, Symbiosis International (Deemed University), Lavale, Pune, Maharashtra, India
,
Shamim A. Shaikh
2   Rajiv Gandhi Institute of IT and Biotechnology, Bharati Vidyapeeth (Deemed to be University), Katraj, Pune, Maharashtra, India
,
Nilesh Shah
3   Department of Surgery and Homeopathic Therapeutics, Bharati Vidyapeeth (Deemed to be University), Homoeopathic Medical College, Katraj, Pune, Maharashtra, India
,
Rashmi S. Tupe 
1   Symbiosis School of Biological Sciences, Symbiosis International (Deemed University), Lavale, Pune, Maharashtra, India
› Author Affiliations Funding This study was funded by the Ministry of Ayurveda, Yoga, and Naturopathy, Unani, Siddha and Homeopathy (AYUSH), Government of India (Grant no: Z. 28015/103/2012-HPC [EMR]-AYUSH).
› Further Information
    Permissions and Reprints

Abstract

Background The growing interest in identifying the mode of action of traditional medicines has strengthened its research. Syzygium jambolanum (Syzyg) is commonly prescribed in homeopathy and is a rich source of phytochemicals.

Objective The present study aims to shed light on the anti-glycation molecular mechanism of Syzyg mother tincture (MT), 30c, and 200c on glycated human serum albumin (HSA) by multi-spectroscopic and microscopic approaches.

Methods The phytochemicals and antioxidant potential of the Syzyg formulations were estimated by the high-performance liquid chromatography and spectroscopic technique, respectively. Glycation was initiated by incubating HSA with methylglyoxal, three Syzyg formulations, and the known inhibitor aminoguanidine in separate tubes at 37°C for 48 hours. The formation of glycation adducts was assessed by spectrofluorometer and affinity chromatography. The structural modifications were analyzed through circular dichroism, Fourier transform infrared spectroscopy, turbidity, 8-anilinonapthalene-1-sulfonic acid fluorescence, and nuclear magnetic resonance. Further, the formation of the aggregates was examined by thioflavin T, native-polyacrylamide gel electrophoresis, and transmission electron microscopy. Additionally, the functional modifications of glycated HSA were determined by esterase-like activity and antioxidant capacity. The binding analysis of Syzyg formulations with glycated HSA was evaluated by surface plasmon resonance (SPR).

Results Syzyg formulations MT, 30c, and 200c contained gallic acid and ellagic acid as major phytochemicals, with concentrations of 16.02, 0.86, and 0.52 µg/mL, and 227.35, 1.35, and 0.84 µg/mL, respectively. Additionally, all three formulations had remarkable radical scavenging ability and could significantly inhibit glycation compared with aminoguanidine. Further, Syzyg formulations inhibited albumin's structural and functional modifications. SPR data showed that Syzyg formulations bind to glycated HSA with an equilibrium dissociation constant of 1.10 nM.

Conclusion Syzyg formulations inhibited the glycation process while maintaining the structural and functional integrity of HSA.

Keywords

albumin - glycation - homeopathy - Syzygium jambolanum

Authors' Contributions

N.S.B.: Investigation, formal analysis, writing original draft. S.R.: Data analysis. S.A.S.: Supervision, project administration. N.S.: Project administration. R.S.T.: Supervision, project administration, validation, review and editing, funding acquisition.




Publication History

Received: 24 January 2023

Accepted: 11 May 2023

Article published online:
19 October 2023

© 2023. Faculty of Homeopathy. This article is published by Thieme.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Giri B, Dey S, Das T, Sarkar M, Banerjee J, Dash SK. Chronic hyperglycemia mediated physiological alteration and metabolic distortion leads to organ dysfunction, infection, cancer progression and other pathophysiological consequences: an update on glucose toxicity. Biomed Pharmacother 2018; 107: 306-328
    CrossrefPubMedGoogle Scholar
  • 2 Chhipa AS, Borse SP, Baksi R, Lalotra S, Nivsarkar M. Targeting receptors of advanced glycation end products (RAGE): preventing diabetes induced cancer and diabetic complications. Pathol Res Pract 2019; 215: 152643
    CrossrefPubMedGoogle Scholar
  • 3 Rhee SY, Kim YS. The role of advanced glycation end products in diabetic vascular complications. Diabetes Metab J 2018; 42: 188-195
    CrossrefPubMedGoogle Scholar
  • 4 Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 2001; 414: 813-820
    CrossrefPubMedGoogle Scholar
  • 5 Nowotny K, Jung T, Höhn A, Weber D, Grune T. Advanced glycation end products and oxidative stress in type 2 diabetes mellitus. Biomolecules 2015; 5: 194-222
    CrossrefPubMedGoogle Scholar
  • 6 Vistoli G, De Maddis D, Cipak A, Zarkovic N, Carini M, Aldini G. Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radic Res 2013; 47 (Suppl. 01) 3-27
    CrossrefPubMedGoogle Scholar
  • 7 Ruiz HH, Ramasamy R, Schmidt AM. Advanced glycation end products: building on the concept of the “common soil” in metabolic disease. Endocrinology 2020; 161: bqz006
    CrossrefPubMedGoogle Scholar
  • 8 Rabbani G, Ahn SN. Structure, enzymatic activities, glycation and therapeutic potential of human serum albumin: a natural cargo. Int J Biol Macromol 2019; 123: 979-990
    CrossrefPubMedGoogle Scholar
  • 9 Zeng ZF, Huang QP, Cai JH. et al. CT-DNA/HSA binding interactions and cytotoxicity activity of a new copper (II) complex. Inorg Chem Commun 2021; 133: 108917
    CrossrefPubMedGoogle Scholar
  • 10 Hajili M, Pour Khalili N, Moradi R, Abdullayev Y. Targeting interface HSA through anti-cancer drugs: molecular modeling and docking. Mater Today Proc 2021; 42: A1-A9
    CrossrefPubMedGoogle Scholar
  • 11 Kohzuma T, Tao X, Koga M. Glycated albumin as biomarker: evidence and its outcomes. J Diabetes Complications 2021; 35: 108040
    CrossrefPubMedGoogle Scholar
  • 12 Rondeau P, Bourdon E. The glycation of albumin: structural and functional impacts. Biochimie 2011; 93: 645-658
    CrossrefPubMedGoogle Scholar
  • 13 Guerin-Dubourg A, Catan A, Bourdon E, Rondeau P. Structural modifications of human albumin in diabetes. Diabetes Metab 2012; 38: 171-178
    CrossrefPubMedGoogle Scholar
  • 14 Neelofar K, Arif Z, Alam K, Ahmad J. Hyperglycemia induced structural and functional changes in human serum albumin of diabetic patients: a physico-chemical study. Mol Biosyst 2016; 12: 2481-2489
    CrossrefPubMedGoogle Scholar
  • 15 Singla R, Abidi SMS, Dar AI, Acharya A. Inhibition of glycation-induced aggregation of human serum albumin by organic–inorganic hybrid nanocomposites of iron oxide-functionalized nanocellulose. ACS Omega 2019; 4: 14805-14819
    CrossrefPubMedGoogle Scholar
  • 16 Annamalai K, Liberta F, Vielberg MT. et al. Common fibril structures imply systemically conserved protein misfolding pathways in vivo . Angew Chem Int Ed Engl 2017; 56: 7510-7514
    CrossrefPubMedGoogle Scholar
  • 17 Thornalley PJ. Use of aminoguanidine (Pimagedine) to prevent the formation of advanced glycation endproducts. Arch Biochem Biophys 2003; 419: 31-40
    CrossrefPubMedGoogle Scholar
  • 18 Stoppa GR, Cesquini M, Roman EAFR, Ogo SH, Torsoni MA. Aminoguanidine prevented impairment of blood antioxidant system in insulin-dependent diabetic rats. Life Sci 2006; 78: 1352-1361
    CrossrefPubMedGoogle Scholar
  • 19 Bolton WK, Cattran DC, Williams ME. et al; ACTION I Investigator Group. Randomized trial of an inhibitor of formation of advanced glycation end products in diabetic nephropathy. Am J Nephrol 2004; 24: 32-40
    CrossrefPubMedGoogle Scholar
  • 20 Nahid S, Mazumder K, Rahman Z, Islam S. Rashid MdH, Kerr PG. Cardio- and hepato-protective potential of methanolic extract of Syzygium cumini (L.) Skeels seeds: a diabetic rat model study. Asian Pac J Trop Biomed 2017; 7: 126-133
    CrossrefPubMedGoogle Scholar
  • 21 Ravi K, Rajasekaran S, Subramanian S. Antihyperlipidemic effect of Eugenia jambolana seed kernel on streptozotocin-induced diabetes in rats. Food Chem Toxicol 2005; 43: 1433-1439
    CrossrefPubMedGoogle Scholar
  • 22 Sharma B, Balomajumder C, Roy P. Hypoglycemic and hypolipidemic effects of flavonoid rich extract from Eugenia jambolana seeds on streptozotocin induced diabetic rats. Food Chem Toxicol 2008; 46: 2376-2383
    CrossrefPubMedGoogle Scholar
  • 23 Sridhar SB, Sheetal UD, Pai MRSM, Shastri MS. Preclinical evaluation of the antidiabetic effect of Eugenia jambolana seed powder in streptozotocin-diabetic rats. Braz J Med Biol Res 2005; 38: 463-468
    CrossrefPubMedGoogle Scholar
  • 24 Ayyanar M, Subash-Babu P, Ignacimuthu S. Syzygium cumini (L.) Skeels, a novel therapeutic agent for diabetes: folk medicinal and pharmacological evidences. Complement Ther Med 2013; 21: 232-243
    CrossrefPubMedGoogle Scholar
  • 25 Badhani B, Sharma N, Kakkar R. Gallic acid: a versatile antioxidant with promising therapeutic and industrial applications. RSC Advances 2015; 5: 27540-27557
    CrossrefPubMedGoogle Scholar
  • 26 Rodrigues-Neto JF, Figueiredo MFS, Faria AA. Prevalence of the use of homeopathy by the population of Montes Claros, Minas Gerais, Brazil. Sao Paulo Med J 2009; 127: 329-334
    CrossrefPubMedGoogle Scholar
  • 27 Tupe RS, Kulkarni A, Adeshara K, Shaikh S, Shah N, Jadhav A. Syzygium jambolanum and Cephalandra indica homeopathic preparations inhibit albumin glycation and protect erythrocytes: an in vitro study. Homeopathy 2015; 104: 197-204
    Article in Thieme ConnectPubMedGoogle Scholar
  • 28 Maiti S, Bera TK, Chatterjee K, Ghosh D. A study of the effect of mother tincture of Syzygium jambolanum on metabolic disorders of streptozotocin induced diabetic male albino rat. Ind J Res Homoeopathy 2014; 8: 129-135
    CrossrefPubMedGoogle Scholar
  • 29 Maiti S, Ali KM, Jana K, Chatterjee K, De D, Ghosh D. Ameliorating effect of mother tincture of Syzygium jambolanum on carbohydrate and lipid metabolic disorders in streptozotocin-induced diabetic rat: homeopathic remedy. J Nat Sci Biol Med 2013; 4: 68-73
    CrossrefPubMedGoogle Scholar
  • 30 Sampath S, Narasimhan A, Chinta R. et al. Effect of homeopathic preparations of Syzygium jambolanum and Cephalandra indica on gastrocnemius muscle of high fat and high fructose-induced type-2 diabetic rats. Homeopathy 2013; 102: 160-171
    Article in Thieme ConnectPubMedGoogle Scholar
  • 31 Priya SH, Prakasan N, Purushothaman J. Antioxidant activity, phenolic-flavonoid content and high-performance liquid chromatography profiling of three different variants of Syzygium cumini seeds: a comparative study. J Intercult Ethnopharmacol 2017; 6: 107-114
    CrossrefPubMedGoogle Scholar
  • 32 Brand-Williams W, Cuvelier ME, Berset C. Use of a free radical method to evaluate antioxidant activity. Lebensm Wiss Technol 1995; 28: 25-30
    CrossrefPubMedGoogle Scholar
  • 33 Ruch RJ, Cheng SJ, Klaunig JE. Prevention of cytotoxicity and inhibition of intercellular communication by antioxidant catechins isolated from Chinese green tea. Carcinogenesis 1989; 10: 1003-1008
    CrossrefPubMedGoogle Scholar
  • 34 Gajahi Soudahome A, Catan A, Giraud P. et al. Glycation of human serum albumin impairs binding to the glucagon-like peptide-1 analogue liraglutide. J Biol Chem 2018; 293: 4778-4791
    CrossrefPubMedGoogle Scholar
  • 35 Jakus V, Bauerová K, Rietbrock N. Effect of aminoguanidine and copper(II) ions on the formation of advanced glycosylation end products. In vitro study on human serum albumin. Arzneimittelforschung 2001; 51: 280-283
    PubMedGoogle Scholar
  • 36 Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the Folin phenol reagent. J Biol Chem 1951; 193: 265-275
    CrossrefPubMedGoogle Scholar
  • 37 Ahmed A, Shamsi A, Khan MS, Husain FM, Bano B. Methylglyoxal induced glycation and aggregation of human serum albumin: biochemical and biophysical approach. Int J Biol Macromol 2018; 113: 269-276
    CrossrefPubMedGoogle Scholar
  • 38 Shamsi A, Amani S, Alam MT, Naeem A. Aggregation as a consequence of glycation: insight into the pathogenesis of arthritis. Eur Biophys J 2016; 45: 523-534
    CrossrefPubMedGoogle Scholar
  • 39 Affinity Chromatography. : a Practical Approach. Dean PDG, Johnson WS, Middle FA. eds Oxford: IRL Press; 1985: 1-14
    Google Scholar
  • 40 Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227: 680-685
    CrossrefPubMedGoogle Scholar
  • 41 Micsonai A, Wien F, Kernya L. et al. Accurate secondary structure prediction and fold recognition for circular dichroism spectroscopy. Proc Natl Acad Sci U S A 2015; 112: E3095-E3103
    CrossrefPubMedGoogle Scholar
  • 42 Wu J, Wang J, Zhang J. et al. Oral delivery of curcumin using silk nano- and microparticles. ACS Biomater Sci Eng 2018; 4: 3885-3894
    CrossrefPubMedGoogle Scholar
  • 43 Pandey NK, Ghosh S, Dasgupta S. Fructose restrains fibrillogenesis in human serum albumin. Int J Biol Macromol 2013; 61: 424-432
    CrossrefPubMedGoogle Scholar
  • 44 Naeem A, Amani S. Deciphering structural intermediates and genotoxic fibrillar aggregates of albumins: a molecular mechanism underlying for degenerative diseases. PLoS One 2013; 8: e54061
    CrossrefPubMedGoogle Scholar
  • 45 Szkudlarek A, Pentak D, Ploch A, Pożycka J, Maciążek-Jurczyk M. In vitro investigation of the interaction of tolbutamide and losartan with human serum albumin in hyperglycemia states. Molecules 2017; 22: 2249
    CrossrefPubMedGoogle Scholar
  • 46 LeVine III H. Thioflavine T interaction with synthetic Alzheimer's disease beta-amyloid peptides: detection of amyloid aggregation in solution. Protein Sci 1993; 2: 404-410
    CrossrefPubMedGoogle Scholar
  • 47 Hirohata M, Ono K, Takasaki J. et al. Anti-amyloidogenic effects of soybean isoflavones in vitro: fluorescence spectroscopy demonstrating direct binding to Aβ monomers, oligomers and fibrils. Biochim Biophys Acta 2012; 1822: 1316-1324
    CrossrefPubMedGoogle Scholar
  • 48 Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 1999; 26: 1231-1237
    CrossrefPubMedGoogle Scholar
  • 49 Löfås S, Johnsson B. A novel hydrogel matrix on gold surfaces in surface plasmon resonance sensors for fast and efficient covalent immobilization of ligands. J Chem Soc Chem Commun 1990; 21: 1526-1528
    CrossrefPubMedGoogle Scholar
  • 50 Malik N, Javaid S, Ashraf W. et al. Long-term supplementation of Syzygium cumini (L.) Skeels concentrate alleviates age-related cognitive deficit and oxidative damage: a comparative study of young vs. old mice. Nutrients 2023; 15: 666
    CrossrefPubMedGoogle Scholar
  • 51 Sousa MM, Lima RMT, Lima A. et al. Antioxidant action and enzyme activity modulation by bioaccessible polyphenols from jambolan (Syzygium cumini (L.) Skeels). Food Chem 2021; 363: 130353
    CrossrefPubMedGoogle Scholar
  • 52 Toshima S, Hirano T, Kunitake H. Comparison of anthocyanins, polyphenols, and antioxidant capacities among raspberry, blackberry, and Japanese wild Rubus species. Sci Hortic (Amsterdam) 2021; 285: 110204
    CrossrefPubMedGoogle Scholar
  • 53 Gong T, Tian D, Hu CY, Guo YR, Meng YH. Improving antioxidant ability of functional emulsifiers by conjugating polyphenols to sodium caseinate. Lebensm Wiss Technol 2022; 154: 112668
    CrossrefPubMedGoogle Scholar
  • 54 Vega J, Álvarez-Gómez F, Güenaga L, Figueroa FL, Gómez-Pinchetti JL. Antioxidant activity of extracts from marine macroalgae, wild-collected and cultivated, in an integrated multi-trophic aquaculture system. Aquaculture 2020; 522: 735088
    CrossrefPubMedGoogle Scholar
  • 55 Bolt HM. High complexity of toxic reactions: parallels between products of oxidative stress and advanced glycation end products. Arch Toxicol 2020; 94: 1373-1374
    CrossrefPubMedGoogle Scholar
  • 56 Li D, Chen Y, Liu Z. Boronate affinity materials for separation and molecular recognition: structure, properties and applications. Chem Soc Rev 2015; 44: 8097-8123
    CrossrefPubMedGoogle Scholar
  • 57 Bhuiyan MNI, Mitsuhashi S, Sigetomi K, Ubukata M. Quercetin inhibits advanced glycation end product formation via chelating metal ions, trapping methylglyoxal, and trapping reactive oxygen species. Biosci Biotechnol Biochem 2017; 81: 882-890
    CrossrefPubMedGoogle Scholar
  • 58 Kerdsomboon K, Chumsawat W, Auesukaree C. Effects of Moringa oleifera leaf extracts and its bioactive compound gallic acid on reducing toxicities of heavy metals and metalloid in Saccharomyces cerevisiae . Chemosphere 2021; 270: 128659
    CrossrefPubMedGoogle Scholar
  • 59 Yeh WJ, Hsia SM, Lee WH, Wu CH. Polyphenols with antiglycation activity and mechanisms of action: a review of recent findings. Yao Wu Shi Pin Fen Xi 2017; 25: 84-92
    PubMedGoogle Scholar
  • 60 Prasanna G, Jing P. Polyphenol binding disassembles glycation-modified bovine serum albumin amyloid fibrils. Spectrochim Acta A Mol Biomol Spectrosc 2021; 246: 119001
    CrossrefPubMedGoogle Scholar
  • 61 Precupas A, Leonties AR, Neacsu A, Sandu R, Popa VT. Gallic acid influence on bovine serum albumin thermal stability. New J Chem 2019; 43: 3891-3898
    CrossrefPubMedGoogle Scholar
  • 62 Zendjabil M. Glycated albumin. Clin Chim Acta 2020; 502: 240-244
    CrossrefPubMedGoogle Scholar
  • 63 Rabbani N, Thornalley PJ. The critical role of methylglyoxal and glyoxalase 1 in diabetic nephropathy. Diabetes 2014; 63: 50-52
    CrossrefPubMedGoogle Scholar
  • 64 Xie L, Wehling RL, Ciftci O, Zhang Y. Formation of complexes between tannic acid with bovine serum albumin, egg ovalbumin and bovine beta-lactoglobulin. Food Res Int 2017; 102: 195-202
    CrossrefPubMedGoogle Scholar
  • 65 Hu B, Shen Y, Adamcik J. et al. Polyphenol-binding amyloid fibrils self-assemble into reversible hydrogels with antibacterial activity. ACS Nano 2018; 12: 3385-3396
    CrossrefPubMedGoogle Scholar
  • 66 Cao P, Raleigh DP. Analysis of the inhibition and remodeling of islet amyloid polypeptide amyloid fibers by flavanols. Biochemistry 2012; 51: 2670-2683
    CrossrefPubMedGoogle Scholar
  • 67 Li J, Du X, Hashim S, Shy A, Xu B. Aromatic–aromatic interactions enable α-helix to β-sheet transition of peptides to form supramolecular hydrogels. J Am Chem Soc 2017; 139: 71-74
    CrossrefPubMedGoogle Scholar
  • 68 Tarannum A, Arif Z, Mustafa M. et al. Studies on the synergistic action of methylglyoxal and peroxynitrite on structure and function of human serum albumin. J Biomol Struct Dyn 2023; 41: 67-80
    CrossrefPubMedGoogle Scholar
  • 69 Arumugam M, Manikandan DB, Dhandapani E. et al. Green synthesis of zinc oxide nanoparticles (ZnO NPs) using Syzygium cumini: potential multifaceted applications on antioxidants, cytotoxic and as nanonutrient for the growth of Sesamum indicum . Environ Technol Innov. 2021; 23: 101653
    CrossrefPubMedGoogle Scholar
  • 70 Dissanayake PK, Wekumbura WGC, Wijeratne AW, Wijesundara DSA. Morphological characterization, antioxidant capacity and diversity of Syzygium cumini trees from Sri Lanka. Hortic Plant J 2022; 8: 53-67
    CrossrefPubMedGoogle Scholar
  • 71 Masaenah E, Elya B, Setiawan H. et al. Antidiabetic activity and acute toxicity of combined extract of Andrographis paniculata, Syzygium cumini, and Caesalpinia sappan . Heliyon 2021; 7: e08561
    CrossrefPubMedGoogle Scholar
  • 72 Sharma M, Prajapati S, Kumar A, Tripathi A, Kumar Gvn, Gupta P. Safety evaluation of Syzygium jambolanum on the development of zebrafish embryos. Ind J Pharm Educ Res. 2021; 55: 198-204
    CrossrefPubMedGoogle Scholar
  • 73 Prabowo BA, Purwidyantri A, Liu KC. Surface plasmon resonance optical sensor: a review on light source technology. Biosensors (Basel) 2018; 8: 67-80
    PubMedGoogle Scholar
  • 74 Zhang L, Cai QY, Cai ZX. et al. Interactions of bovine serum albumin with anti-cancer compounds using a proteOn XPR36 array biosensor and molecular docking. Molecules 2016; 21: 1706
    CrossrefPubMedGoogle Scholar
  • 75 Demangeat JL. NMR water proton relaxation in unheated and heated ultrahigh aqueous dilutions of histamine: evidence for an air-dependent supramolecular organization of water. J Mol Liq 2009; 144: 32-39
    CrossrefPubMedGoogle Scholar
  • 76 Esposito F, Wolf U, Baumgartner S. NMR relaxation time investigation of highly diluted aqueous solutions of silica-lactose. J Mol Liq 2021; 337: 115975
    CrossrefPubMedGoogle Scholar
  • 77 Nain AK, Droliya P, Manchanda RK, Khurana A, Nayak D. Physicochemical studies of homoeopathic formulations (extremely diluted solutions) of acidum salicylicum in ethanol by using volumetric, acoustic, viscometric and refractive index measurements at 298.15, 308.15 and 318.15K. J Mol Liq 2016; 215: 680-690
    CrossrefPubMedGoogle Scholar
  • 78 Nain AK, Droliya P, Manchanda RK, Khurana A, Nayak D. Physicochemical studies of extremely diluted solutions (homoeopathic formulations) of sulphur in ethanol by using volumetric, acoustic, viscometric and refractive index measurements at different temperatures. J Mol Liq 2015; 211: 1082-1094
    CrossrefPubMedGoogle Scholar