ACS Publications. Most Trusted. Most Cited. Most Read
Redox-Active Bis(phenolate) N-Heterocyclic Carbene [OCO] Pincer Ligands Support Cobalt Electron Transfer Series Spanning Four Oxidation States

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:Inorg. Chem. 2017, 56, 20, 12421-12435
    Article

    Redox-Active Bis(phenolate) N-Heterocyclic Carbene [OCO] Pincer Ligands Support Cobalt Electron Transfer Series Spanning Four Oxidation States
    Click to copy article linkArticle link copied!

    View Author Information
    † School of Chemistry and Biochemistry, Georgia Institute of Technology, Atlanta, Georgia 30332-0400, United States
    ‡ Van ’t Hoff Institute for Molecular Sciences (HIMS), University of Amsterdam (UvA), Science Park 904, 1098 XH Amsterdam, The Netherlands
    § Department of Chemistry, Colorado State University, Fort Collins, Colorado 80523-1872, United States
    ∥ X-ray Crystallography Center, Department of Chemistry, Emory University, 1515 Dickey Drive, Atlanta, Georgia 30322, United States
    *E-mail for M.P.S.: [email protected]
    *E-mail for B.d.B.: [email protected]
    *E-mail for J.D.S.: [email protected]
    Other Access OptionsSupporting Information (1)

    Inorganic Chemistry

    Cite this: Inorg. Chem. 2017, 56, 20, 12421–12435
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.inorgchem.7b01906
    Published October 2, 2017
    Copyright © 2017 American Chemical Society
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    A new family of low-coordinate Co complexes supported by three redox-noninnocent tridentate [OCO] pincer-type bis(phenolate) N-heterocyclic carbene (NHC) ligands are described. Combined experimental and computational data suggest that the charge-neutral four-coordinate complexes are best formulated as Co(II) centers bound to closed-shell [OCO]2– dianions, of the general formula [(OCO)CoIIL] (where L is a solvent-derived MeCN or THF). Cyclic voltammograms of the [(OCO)CoIIL] complexes reveal three oxidations accessible at potentials below 1.2 V vs Fc+/Fc, corresponding to generation of formally Co(V) species, but the true physical/spectroscopic oxidation states are much lower. Chemical oxidations afford the mono- and dications of the imidazoline NHC-derived complex, which were examined by computational and magnetic and spectroscopic methods, including single-crystal X-ray diffraction. The metal and ligand oxidation states of the monocationic complex are ambiguous; data are consistent with formulation as either [(SOCO)CoIII(THF)2]+ containing a closed-shell [SOCO]2– diphenolate ligand bound to a S = 1 Co(III) center, or [(SOCO•)CoII(THF)2]+ with a low-spin Co(II) ion ferromagnetically coupled to monoanionic [SOCO•]− containing a single unpaired electron distributed across the [OCO] framework. The dication is best described as [(SOCO0)CoII(THF)3]2+, with a single unpaired electron localized on the d7 Co(II) center and a doubly oxidized, charge-neutral, closed-shell SOCO0 ligand. The combined data provide for the first time unequivocal and structural evidence for [OCO] ligand redox activity. Notably, varying the degree of unsaturation in the NHC backbone shifts the ligand-based oxidation potentials by up to 400 mV. The possible chemical origins of this unexpected shift, along with the potential utility of the [OCO] pincer ligands for base-metal-mediated organometallic coupling catalysis, are discussed.

    Copyright © 2017 American Chemical Society

    Subjects

    what are subjects

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.7b01906.

    • Complete X-ray structure reports for [(SOCO)Co(THF)], [(OCO)Co(MeCN)], [(SOCO)Co(MeCN)], [(PhOCO)Co(MeCN)], [(SOCO)Co(THF)2][BPh4], and [(SOCO)Co(THF)3][PF6]2 and Cartesian coordinates of the DFT optimized geometries of 1–3 (PDF)

    Accession Codes

    CCDC 1563838–1563843 contain the supplementary crystallographic data for this paper. These data can be obtained free of charge via www.ccdc.cam.ac.uk/data_request/cif, or by emailing [email protected], or by contacting The Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge CB2 1EZ, UK; fax: +44 1223 336033.

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai
    powered by  Scite

    This article is cited by 52 publications.

    1. Sakthi Raje, Subhash Garhwal, Katarzyna Młodzikowska-Pieńko, Tofayel Sheikh Mohammad, Ron Raphaeli, Natalia Fridman, Linda J. W. Shimon, Renana Gershoni-Poranne, Graham de Ruiter. N2 Dissociation vs Reversible 1,2-Methyl Migration in PCNHCP Cobalt(I) Complexes in the Stereoselective Isomerization (E/Z) of Allyl Ethers. JACS Au 2024, 4 (11) , 4234-4248. https://doi.org/10.1021/jacsau.4c00529
    2. Lisa Gravogl, Dustin Kass, Oliver Pyschny, Frank W. Heinemann, Michael Haumann, Sagie Katz, Peter Hildebrandt, Holger Dau, Abinash Swain, Ricardo García-Serres, Kallol Ray, Dominik Munz, Karsten Meyer. A bis-Phenolate Carbene-Supported bis-μ-Oxo Iron(IV/IV) Complex with a [FeIV(μ-O)2FeIV] Diamond Core Derived from Dioxygen Activation. Journal of the American Chemical Society 2024, 146 (42) , 28757-28769. https://doi.org/10.1021/jacs.4c07582
    3. Abdollah Neshat, Ali Mousavizadeh Mobarakeh, Mohammad Reza Yousefshahi, Fahimeh Varmaghani, Michal Dusek, Vaclav Eigner, Monika Kucerakova. Introducing Novel Redox-Active Bis(phenolate) N-Heterocyclic Carbene Proligands: Investigation of Their Coordination to Fe(II)/Fe(III) and Their Catalytic Activity in Transfer Hydrogenation of Carbonyl Compounds. ACS Omega 2024, 9 (23) , 25135-25145. https://doi.org/10.1021/acsomega.4c02602
    4. Christopher S. Kuehner, Andrew G. Hill, Caleb F. Harris, Christian A. Owens, John Bacsa, Jake D. Soper. Catalytic C–H Trifluoromethylation of Arenes and Heteroarenes via Visible Light Photoexcitation of a Co(III)–CF3 Complex. ACS Catalysis 2023, 13 (20) , 13607-13617. https://doi.org/10.1021/acscatal.3c03832
    5. Romain Kunert, Christian Philouze, Olivier Jarjayes, Tim Storr, Fabrice Thomas. Single-Oxidation of Ni(II) Complexes of Bidentate Fused N-Heterocyclic Carbene–Phenol Conjugates. Organometallics 2023, 42 (13) , 1550-1560. https://doi.org/10.1021/acs.organomet.3c00140
    6. Sophie W. Anferov, Alexander S. Filatov, John S. Anderson. Cobalt-Catalyzed Hydrogenation Reactions Enabled by Ligand-Based Storage of Dihydrogen. ACS Catalysis 2022, 12 (16) , 9933-9943. https://doi.org/10.1021/acscatal.2c02467
    7. Ranjeesh Thenarukandiyil, Eno Paenurk, Anthony Wong, Natalia Fridman, Amir Karton, Raanan Carmieli, Gabriel Ménard, Renana Gershoni-Poranne, Graham de Ruiter. Extensive Redox Non-Innocence in Iron Bipyridine-Diimine Complexes: a Combined Spectroscopic and Computational Study. Inorganic Chemistry 2021, 60 (23) , 18296-18306. https://doi.org/10.1021/acs.inorgchem.1c02925
    8. Kate A. Jesse, Sophie W. Anferov, Kelsey A. Collins, Juan A. Valdez-Moreira, Maia E. Czaikowski, Alexander S. Filatov, John S. Anderson. Direct Aerobic Generation of a Ferric Hydroperoxo Intermediate Via a Preorganized Secondary Coordination Sphere. Journal of the American Chemical Society 2021, 143 (43) , 18121-18130. https://doi.org/10.1021/jacs.1c06911
    9. David Rendón-Nava, Deyanira Angeles-Beltrán, Arnold L. Rheingold, Daniel Mendoza-Espinosa. Palladium(II) Complexes of a Neutral CCC-Tris(N-heterocyclic carbene) Pincer Ligand: Synthesis and Catalytic Applications. Organometallics 2021, 40 (13) , 2166-2177. https://doi.org/10.1021/acs.organomet.1c00324
    10. Subhash Garhwal, Alexander Kaushansky, Natalia Fridman, Linda J. W. Shimon, Graham de Ruiter. Facile H/D Exchange at (Hetero)Aromatic Hydrocarbons Catalyzed by a Stable Trans-Dihydride N-Heterocyclic Carbene (NHC) Iron Complex. Journal of the American Chemical Society 2020, 142 (40) , 17131-17139. https://doi.org/10.1021/jacs.0c07689
    11. Lisa Gravogl, Frank W. Heinemann, Dominik Munz, Karsten Meyer. An Iron Pincer Complex in Four Oxidation States. Inorganic Chemistry 2020, 59 (8) , 5632-5645. https://doi.org/10.1021/acs.inorgchem.0c00355
    12. Marc Baltrun, Fabian A. Watt, Roland Schoch, Stephan Hohloch. Dioxo-, Oxo-imido-, and Bis-imido-Molybdenum(VI) Complexes with a Bis-phenolate-NHC Ligand. Organometallics 2019, 38 (19) , 3719-3729. https://doi.org/10.1021/acs.organomet.9b00472
    13. Romain Kunert, Christian Philouze, Olivier Jarjayes, Fabrice Thomas. Stable M(II)-Radicals and Nickel(III) Complexes of a Bis(phenol) N-Heterocyclic Carbene Chelated to Group 10 Metal Ions. Inorganic Chemistry 2019, 58 (12) , 8030-8044. https://doi.org/10.1021/acs.inorgchem.9b00784
    14. Andreas A. Danopoulos, Thomas Simler, Pierre Braunstein. N-Heterocyclic Carbene Complexes of Copper, Nickel, and Cobalt. Chemical Reviews 2019, 119 (6) , 3730-3961. https://doi.org/10.1021/acs.chemrev.8b00505
    15. Lukas Alig, Maximilian Fritz, Sven Schneider. First-Row Transition Metal (De)Hydrogenation Catalysis Based On Functional Pincer Ligands. Chemical Reviews 2019, 119 (4) , 2681-2751. https://doi.org/10.1021/acs.chemrev.8b00555
    16. Jun Cheng, Lijun Wang, Peng Wang, Liang Deng. High-Oxidation-State 3d Metal (Ti–Cu) Complexes with N-Heterocyclic Carbene Ligation. Chemical Reviews 2018, 118 (19) , 9930-9987. https://doi.org/10.1021/acs.chemrev.8b00096
    17. Nicole M. Mews, Gerald Hörner, Hartmut Schubert, Andreas Berkefeld. Tuning of Thiyl/Thiolate Complex Near-Infrared Chromophores of Platinum through Geometrical Constraints. Inorganic Chemistry 2018, 57 (16) , 9670-9682. https://doi.org/10.1021/acs.inorgchem.8b00122
    18. Romain Kunert, Diego Martelino, Samyadeb Mahato, Nicholas M. Hein, Jason Pulfer, Christian Philouze, Olivier Jarjayes, Fabrice Thomas, Tim Storr. Investigating the formation of metal nitride complexes employing a tetradentate bis-carbene bis-phenolate ligand. Dalton Transactions 2025, 54 (2) , 616-630. https://doi.org/10.1039/D4DT01765J
    19. Kate A. Jesse, John S. Anderson. Leveraging ligand-based proton and electron transfer for aerobic reactivity and catalysis. Chemical Science 2024, 15 (40) , 16409-16423. https://doi.org/10.1039/D4SC03896G
    20. Fengkai He, Konstantinos P. Zois, Demeter Tzeli, Andreas A. Danopoulos, Pierre Braunstein. N-heterocyclic carbenes as bridgehead donors in metal pincer complexes. Coordination Chemistry Reviews 2024, 514 , 215757. https://doi.org/10.1016/j.ccr.2024.215757
    21. P. A. Petrov, S. A. Nikolaevskii, E. A. Filippova, N. B. Kompankov, T. S. Sukhikh, M. A. Kiskin, M. N. Sokolov, I. L. Eremenko. New Polymorph of 1,3-Bis(2,6-di-isopropylphenyl)-4,5-Dichloroimidazole-2-Ylidene and a Cobalt Complex with this Compound. Journal of Structural Chemistry 2024, 65 (1) , 117-124. https://doi.org/10.1134/S0022476624010116
    22. Abdollah Neshat, Rahimeh Khezri, Mohammad Reza Yousefshahi, Mohammad Gholinejad, Fahimeh Varmaghani. Carbon−Sulfur Coupling Reactions Catalyzed by Nickel(II) N‐Heterocyclic Carbene Complexes. European Journal of Inorganic Chemistry 2023, 26 (36) https://doi.org/10.1002/ejic.202300437
    23. Ilya K. Mikhailov, Zufar N. Gafurov, Alexey A. Kagilev, Vladimir I. Morozov, Artyom O. Kantyukov, Ekaterina M. Zueva, Gumar R. Ganeev, Ilyas F. Sakhapov, Asiya V. Toropchina, Igor A. Litvinov, Galina A. Gurina, Alexander A. Trifonov, Oleg G. Sinyashin, Dmitry G. Yakhvarov. Redox Chemistry of Pt(II) Complex with Non-Innocent NHC Bis(Phenolate) Pincer Ligand: Electrochemical, Spectroscopic, and Computational Aspects. Catalysts 2023, 13 (9) , 1291. https://doi.org/10.3390/catal13091291
    24. P. A. Petrov, S. A. Nikolaevskii, D. S. Yambulatov, T. S. Sukhikh, A. A. Starikova, M. A. Kiskin, M. N. Sokolov, I. L. Eremenko. Heteroleptic Cobalt Complexes with Abnormally Coordinated N-Heterocyclic Carbene. Russian Journal of Coordination Chemistry 2023, 49 (7) , 407-413. https://doi.org/10.1134/S1070328423600274
    25. P. A. Petrov, S. A. Nikolaevskii, D. S. Yambulatov, T. S. Sukhikh, A. A. Starikova, M. A. Kiskin, M. N. Sokolov, I. L. Eremenko. Heteroleptic Cobalt Complexes with Abnormally Coordinated N-Heterocyclic Carbene. Координационная химия 2023, 49 (7) , 398-405. https://doi.org/10.31857/S0132344X22600527
    26. Giacomo Rigoni, Pamela V. S. Nylund, Martin Albrecht. Manganese( iii ) complexes stabilized with N-heterocyclic carbene ligands for alcohol oxidation catalysis. Dalton Transactions 2023, 52 (23) , 7992-8002. https://doi.org/10.1039/D3DT01013A
    27. Mirko Ruamps, Stéphanie Bastin, Lionel Rechignat, Alix Sournia-Saquet, Laure Vendier, Noël Lugan, Jean-Marie Mouesca, Dmitry A. Valyaev, Vincent Maurel, Vincent César. Redox-Switchable Behavior of Transition-Metal Complexes Supported by Amino-Decorated N-Heterocyclic Carbenes. Molecules 2022, 27 (12) , 3776. https://doi.org/10.3390/molecules27123776
    28. Benjamin Wittwer, Nicole Dickmann, Stephan Berg, Daniel Leitner, Lorenzo Tesi, David Hunger, Raphael Gratzl, Joris van Slageren, Nicolas I. Neuman, Dominik Munz, Stephan Hohloch. A mesoionic carbene complex of manganese in five oxidation states. Chemical Communications 2022, 58 (41) , 6096-6099. https://doi.org/10.1039/D2CC00097K
    29. Fengkai He, Christophe Gourlaouen, Huan Pang, Pierre Braunstein. Influence of the Flexibility of Nickel PCP‐Pincer Complexes on C−H and P−C Bond Activation and Ethylene Reactivity: A Combined Experimental and Theoretical Investigation. Chemistry – A European Journal 2022, 28 (10) https://doi.org/10.1002/chem.202104234
    30. Noufal Kandoth, Miguel Claros, Nuria Rodriguez, Julio Lloret-Fillol. Photoinduced Electron-Transfer in First-Row Transition Metal Complexes. 2022, 493-546. https://doi.org/10.1007/978-3-030-63713-2_20
    31. Errikos Kounalis, Daniël L.J. Broere. Redox-Active Ligands in Organometallic Chemistry. 2022, 421-441. https://doi.org/10.1016/B978-0-12-820206-7.00028-7
    32. Aleksa Radović, Shilpa Bhatia, Michael L. Neidig. Characterization Methods for Paramagnetic Organometallic Complexes. 2022, 135-175. https://doi.org/10.1016/B978-0-12-820206-7.00059-7
    33. Thomas Simler, Andreas A. Danopoulos, Pierre Braunstein. N-Heterocyclic Carbene Complexes of Cobalt. 2022, 632-758. https://doi.org/10.1016/B978-0-12-820206-7.00109-8
    34. Fabian A. Watt, Benedikt Sieland, Nicole Dickmann, Roland Schoch, Regine Herbst-Irmer, Holger Ott, Jan Paradies, Dirk Kuckling, Stephan Hohloch. Coupling of CO 2 and epoxides catalysed by novel N -fused mesoionic carbene complexes of nickel( ii ). Dalton Transactions 2021, 50 (46) , 17361-17371. https://doi.org/10.1039/D1DT03311E
    35. Sébastien Le Roux, Guido Ori, Stéphane Bellemin-Laponnaz, Mauro Boero. Tridentate complexes of group 4 bearing bis-aryloxide N-heterocyclic carbene ligand: Structure, spin density and charge states. Chemical Physics Letters 2021, 781 , 138888. https://doi.org/10.1016/j.cplett.2021.138888
    36. Lakshmi Suresh, Jone Finnstad, Karl W. Törnroos, Erwan Le Roux. Bis(phenolate)-functionalized N-heterocyclic carbene complexes of oxo- and imido-vanadium(V). Inorganica Chimica Acta 2021, 521 , 120301. https://doi.org/10.1016/j.ica.2021.120301
    37. Yidan Wang, Bo Zhang, Shuai Guo. Transition Metal Complexes Supported by N‐Heterocyclic Carbene‐Based Pincer Platforms: Synthesis, Reactivity and Applications. European Journal of Inorganic Chemistry 2021, 2021 (3) , 188-204. https://doi.org/10.1002/ejic.202000911
    38. Lakshmi Suresh, Ralte Lalrempuia, Jonas B. Ekeli, Francis Gillis-D’Hamers, Karl W. Törnroos, Vidar R. Jensen, Erwan Le Roux. Unsaturated and Benzannulated N-Heterocyclic Carbene Complexes of Titanium and Hafnium: Impact on Catalysts Structure and Performance in Copolymerization of Cyclohexene Oxide with CO2. Molecules 2020, 25 (19) , 4364. https://doi.org/10.3390/molecules25194364
    39. Andreas A. Danopoulos, Pierre Braunstein, Jörg Saßmannshausen, David Pugh, Joseph A. Wright. “Pincer” Pyridine–Dicarbene–Iridium and ‐Ruthenium Complexes and Derivatives Thereof. European Journal of Inorganic Chemistry 2020, 2020 (35) , 3359-3369. https://doi.org/10.1002/ejic.202000429
    40. Irina N. Meshcheryakova, Kseniya V. Arsenyeva, Georgy K. Fukin, Vladimir K. Cherkasov, Alexandr V. Piskunov. Stable N-heterocyclic carbene derivatives of copper(i) and silver(i) containing radical anion redox active ligands. Mendeleev Communications 2020, 30 (5) , 592-595. https://doi.org/10.1016/j.mencom.2020.09.013
    41. Rachid Taakili, Yves Canac. NHC Core Pincer Ligands Exhibiting Two Anionic Coordinating Extremities. Molecules 2020, 25 (9) , 2231. https://doi.org/10.3390/molecules25092231
    42. Jarl Ivar van der Vlugt. Redox-Active Pincer Ligands. 2020https://doi.org/10.1007/3418_2020_68
    43. Marta Martín, Eduardo Sola. Recent advances in the chemistry of group 9—Pincer organometallics. 2020, 79-193. https://doi.org/10.1016/bs.adomc.2019.09.002
    44. Vladimir B. Arion. Coordination chemistry of S-substituted isothiosemicarbazides and isothiosemicarbazones. Coordination Chemistry Reviews 2019, 387 , 348-397. https://doi.org/10.1016/j.ccr.2019.02.013
    45. Jarl Ivar van der Vlugt. Radical‐Type Reactivity and Catalysis by Single‐Electron Transfer to or from Redox‐Active Ligands. Chemistry – A European Journal 2019, 25 (11) , 2651-2662. https://doi.org/10.1002/chem.201802606
    46. Simon Sung, Qingyang Wang, Tobias Krämer, Rowan D. Young. Synthesis and reactivity of a PC carbene P cobalt( i ) complex: the missing link in the cobalt PXP pincer series (X = B, C, N). Chemical Science 2018, 9 (43) , 8234-8241. https://doi.org/10.1039/C8SC02782J
    47. Jacob Spencer, Andrea Folli, Emma Richards, Damien M. Murphy. Applications of electron paramagnetic resonance spectroscopy for interrogating catalytic systems. 2018, 130-170. https://doi.org/10.1039/9781788013888-00130
    48. Xiaoyu Ren, Marcel Wesolek, Pierre Braunstein. Nickel(II) Complexes with Tritopic N imine C NHC N amine Pincer Ligands. Chemistry – A European Journal 2018, 24 (55) , 14794-14801. https://doi.org/10.1002/chem.201802969
    49. Catherine Gandara, Christian Philouze, Olivier Jarjayes, Fabrice Thomas. Coordination chemistry of a redox non-innocent NHC bis(phenolate) pincer ligand with nickel(II). Inorganica Chimica Acta 2018, 482 , 561-566. https://doi.org/10.1016/j.ica.2018.06.046
    50. Caleb F. Harris, Christopher S. Kuehner, John Bacsa, Jake D. Soper. Photoinduced Cobalt(III)−Trifluoromethyl Bond Activation Enables Arene C−H Trifluoromethylation. Angewandte Chemie 2018, 130 (5) , 1325-1329. https://doi.org/10.1002/ange.201711693
    51. Caleb F. Harris, Christopher S. Kuehner, John Bacsa, Jake D. Soper. Photoinduced Cobalt(III)−Trifluoromethyl Bond Activation Enables Arene C−H Trifluoromethylation. Angewandte Chemie International Edition 2018, 57 (5) , 1311-1315. https://doi.org/10.1002/anie.201711693
    52. Mirko Ruamps, Stéphanie Bastin, Lionel Rechignat, Alix Sournia-Saquet, Dmitry A. Valyaev, Jean-Marie Mouesca, Noël Lugan, Vincent Maurel, Vincent César. Unveiling the redox-active character of imidazolin-2-thiones derived from amino-substituted N-heterocyclic carbenes. Chemical Communications 2018, 54 (55) , 7653-7656. https://doi.org/10.1039/C8CC03934H
    Download PDF
    Go to Inorganic Chemistry
    Get e-Alerts
    Get e-Alerts

    Inorganic Chemistry

    Cite this: Inorg. Chem. 2017, 56, 20, 12421–12435
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.inorgchem.7b01906
    Published October 2, 2017
    Copyright © 2017 American Chemical Society
    Request reuse permissions

    Article Views

    4350

    Altmetric

    -

    Citations

    52
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.