FRINK Linked Data Fragments server

Matches in SemOpenAlex for { <https://semopenalex.org/work/W1987282998> ?p ?o ?g. }

• W1987282998 endingPage "711" @default.
• W1987282998 startingPage "709" @default.
• W1987282998 abstract "HomeCirculationVol. 123, No. 7Remote Ischemic Preconditioning Free AccessEditorialPDF/EPUBAboutView PDFView EPUBSections ToolsAdd to favoritesDownload citationsTrack citationsPermissions ShareShare onFacebookTwitterLinked InMendeleyReddit Jump toFree AccessEditorialPDF/EPUBRemote Ischemic PreconditioningMaking the Brain More Tolerant, Safely and Inexpensively Michael A. Moskowitz and Christian Waeber Michael A. MoskowitzMichael A. Moskowitz From the Stroke and Neurovascular Regulation Laboratory, Massachusetts General Hospital/Harvard Medical School, Boston, MA. Search for more papers by this author and Christian WaeberChristian Waeber From the Stroke and Neurovascular Regulation Laboratory, Massachusetts General Hospital/Harvard Medical School, Boston, MA. Search for more papers by this author Originally published7 Feb 2011https://doi.org/10.1161/CIRCULATIONAHA.110.009688Circulation. 2011;123:709–711Other version(s) of this articleYou are viewing the most recent version of this article. Previous versions: January 1, 2011: Previous Version 1 Circulatory arrest and stroke are among the leading causes of death and disability worldwide, and they are difficult to treat. Only a limited number of therapeutic approaches have reached the bedside (eg, hypothermia and recombinant tissue plasminogen activator)1 and, unfortunately, relatively few patients are eligible. Virtually all experimental compounds tested so far have failed at some stage of translational development. Preconditioning is an attractive strategy that makes the brain and other visceral organs relatively resistant to tissue injury. It develops when a noxious stimulus, below the damage threshold, leads to reduced tissue injury on subsequent challenge with a stimulus given above injury threshold. It is an appealing strategy to identify novel endogenous protective mechanisms and, as demonstrated by Jensen, Loukogeorgakis, and their colleagues in this issue of Circulation,2 it may prove useful to prevent brain damage in the clinical context when there is a high probability of cerebral ischemia (eg, before high-risk surgery or in patients with subarachnoid hemorrhage).Article see p 714Various types of preconditioning stimuli have been used experimentally to protect brain, heart, retina, liver, kidney, and other organs.3 Some use ischemic preconditioning, in which the blood supply to a target organ is temporarily interrupted before introducing a longer infarct-generating insult that would ordinarily produce infarction; other studies use hypoxic preconditioning, in which animals are exposed to oxygen levels around 8% to 9% for a few hours. But ischemia and hypoxia are just 2 examples in a larger list of strategies that induce tolerance to brain injury: hypoglycemia, hypoxia, kainate-induced seizures, and exposure to volatile anesthetics, to name a few.4 Preconditioning can protect the brain either rapidly after stimulation (known as early, first window, or classical preconditioning) or after a 24-hour delay to induce protein synthesis-dependent protection lasting up to 96 hours (known as delayed or second window preconditioning).Because of its longer duration, delayed preconditioning has attracted more preclinical attention, with the hope that pharmacological approaches may mimic the powerful late-phase protection. But clinically, early preconditioning is more appealing because it can be applied, at least in theory, right before procedures that carry a high risk of cardiac or brain complications. Delivering a preconditioning stimulus to the brain itself would be more challenging and less practical than to other organs, and it is therefore likely to be less useful than alternative strategies. The notion that tolerance can be achieved in the brain by inducing ischemia-reperfusion in a distant (remote) nonvital organ is consistent with the idea that transient ischemia in a visceral organ or tissue (eg, heart, kidney, intestine, or skeletal muscle) can protect remote organs against the effects of extended subsequent ischemia-reperfusion injury.In this issue of Circulation, Jensen and colleagues describe their experience with remote ischemic preconditioning (rIPC) in hypothermic circulatory arrest in piglets.2 Their results in this small but convincing study speak to the potential utility of rIPC during elective or planned procedures that pose a risk to the integrity of vital organs and tissues. They used biochemical, electrophysiological, behavioral, and pathological outcome measures in a randomized group allocation protocol in which the surgeons and postoperative evaluators were blinded to the treatment group assignment. Jensen and colleagues found statistically significant improvement in brain as well as cardiac function after rIPC during the rewarming phase and continuing for at least 7 days after cardiac arrest. They found tissue protection in 2 brain regions exquisitely sensitive to global ischemia, hippocampus, and cortex, as well as electrophysiological and behavioral evidence for better brain function than in the controls. Edema and blood brain barrier disruption were also diminished. The conditioning stimulus used by Jensen and colleagues appears relatively safe, easy, and efficient to administer. Taken together, these results help to solidify remote preconditioning as a potentially useful strategy to improve central nervous system function.The study by Jensen and colleagues also adds to an emerging literature on rIPC in experimental cerebral ischemia indicating that rIPC may not only preserve brain tissue after global ischemia but after focal ischemic insult as well.5 The studies are notable for the number of different limb ischemia protocols that were used, including 3 cycles of 10 minutes of bilateral femoral artery occlusion followed by recirculation, 15 or 30 minutes of a single occlusion and 30 minutes with a single occlusion, and 4 cycles of 5 minutes of ischemia followed by 5 minutes of occlusion.6 The interval between the preconditioning event and global ischemia also varied (immediately after or with an interval of 15 minutes or 48 hours), although a recent study failed to see protection when the interval between remote ischemia reperfusion extended to 48 hours prior to transient global cerebral ischemia in rats.7 Clearly, more work will be needed to clarify the issues of protocol optimization for brain (eg, ideal timing and magnitude of limb ischemia-reperfusion) and to determine whether remote preconditioning differs sufficiently or mechanistically from prior postconditioning strategies.4 Clinical trials should be approached cautiously to avoid the myriad of pitfalls that have plagued translational stroke research, a topic that has been debated extensively.8,9More information is available regarding rIPC in organs other than brain, and experimental studies have now begun to translate these findings to the clinic in several randomized trials with exciting, albeit preliminary results. For example, rIPC was associated with reduced incidence of postoperative myocardial infarction and renal impairment in patients undergoing elective abdominal aortic aneurysm repair.10 Heart protection after rIPC was also reported during coronary stenting11 and in controlled trials to reduce infarct size after myocardial infarction.12 rIPC also protected the heart during cardiac surgery using cardiopulmonary bypass in children13 and improved systemic tolerance to ischemia-reperfusion in a prospective randomized, controlled study of 70 infants undergoing open heart surgery.14 Encouraging results were also reported in a retrospective secondary analysis assessing the impact of rIPC on acute kidney injury during cardiac surgery. In this study with acknowledged shortcomings, the results show a significant decrease in the risk of acute kidney injury in 78 nondiabetic patients subjected to transient forearm ischemia prior to undergoing elective coronary artery bypass graft surgery.15 Ultimately, the clinical utility of such a seemingly safe and inexpensive procedure will be determined by larger randomized, controlled trials (eg, Remote Ischemic Preconditioning in Cardiac Surgery Trial [Remote IMPACT], ClinicalTrials.gov identifier: NCT01071265; or Remote Ischemic Preconditioning for Heart Surgery [RIPHeart-Study] ClinicalTrials.gov identifier: NCT01067703).The signaling pathways that may be involved in the protection afforded by rIPC are largely undefined, but more than likely pleiotropic, multifactorial, and redundant. Similar to direct ischemic preconditioning, many studies have shown the existence of 2 phases of protection by rIPC, and the delayed phase for both seems to be protein synthesis-dependent.6 These and other studies suggest that direct and remote ischemic preconditioning are likely to share at least some overlapping signaling pathways. For example, both rIPC and direct ischemic preconditioning promote tolerance in the heart or brain via protein kinase Cε activation leading to the opening of mitochondrial ATP-dependent K+ channels (KATP).16 Mitochondrial KATP channel opening inhibits the formation of the mitochondrial permeability transition pore, a key step leading to cell death. The mitochondrial permeability transition pore opens during the first minutes of reperfusion and induces cell death by uncoupling oxidative phosphorylation and promoting mitochondrial swelling.1 Other signaling pathways involved in direct ischemic preconditioning, such as the recently implicated polycomb proteins in brain,17,18 have been reviewed elsewhere.3,4A unique and intriguing aspect of rIPC is the transfer of the protective stimulus from the remote to the target organ. A role has been hypothesized for biological factors such as bradykinin, adenosine, nitric oxide/calcitonin gene-related peptide, opioids, or endocannabinoids released by remote tissues. These factors may be carried via circulation to the target organ as rIPC is observed following transient (but not permanent) occlusion of the preconditioning tissue, and following transfer of coronary effluent between isolated hearts.19 These studies also point to the possibility that putative protective humoral factors might be identified and targeted clinically. There is also evidence that factors released by the preconditioning organ affect the target organ via afferent and efferent neural connections that may involve autonomic and sensory pathways. Whether similar pathways play a role in rIPC within brain, however, is currently unknown.6Finally, rIPC may be part of a systemic protective response associated with the suppression of deleterious inflammatory processes evoked by remote organ ischemia and reperfusion. Neutrophil infiltration, adhesion, and activation play an important role in early and late ischemia/reperfusion injury,20 and rIPC in humans reduces neutrophil activation through reduced expression of neutrophil CD11b and platelet-neutrophil complexes. rIPC may activate signal pathways in neutrophils modulating the release of proinflammatory cytokines and the expression of adhesion markers. Neural, humoral and antiinflammatory pathways probably interact with each other and are not necessarily mutually exclusive16; the relative importance of each pathway may depend on the duration of preconditioning ischemia, the tissue or organ generating the preconditioning stimulus,19 and the particular species tested.Based on the best case scenario, remote preconditioning strategies may become applicable to a host of acute neurovascular insults (surgical or otherwise) that negatively impact the integrity of the nervous system. rIPC will gain even wider application if conditioning protects the nervous system even after sustaining injury to a vital organ, as appears to be the case for myocardial protection (remote ischemic postconditioning or RIPost).16 As a final thought, it is tempting to forecast that remote preconditioning might become an established clinical paradigm of notable importance not only in disease but also in health, based on the recent demonstration that rIPC boosted maximal performance in highly trained athletes.21DisclosuresNone.FootnotesThe opinions expressed in this article are not necessarily those of the editors or of the American Heart Association.Correspondence to Michael A. Moskowitz, MD, Massachusetts General Hospital, CNY149-6403, 149 13th Street, Charlestown, MA 02129. E-mail [email protected]mgh.harvard.eduReferences1. Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron. 2010; 67: 181– 198. CrossrefMedlineGoogle Scholar2. Jensen HA, Loukogeorgakis S, Yannopoulos F, Rimpiläinen E, Petzold A, Tuominen H, Lepola P, MacAllister RJ, Deanfield JE, Mäkelä T, Alestalo K, Kiviluoma K, Anttila V, Tsang V, Juvonen T. Remote ischemic preconditioning protects the brain against injury after hypothermic circulatory arrest. Circulation. 2011; 123: 714– 721. LinkGoogle Scholar3. Sharp FR, Ran R, Lu A, Tang Y, Strauss KI, Glass T, Ardizzone T, Bernaudin M. Hypoxic preconditioning protects against ischemic brain injury. NeuroRx. 2004; 1: 26– 35. CrossrefMedlineGoogle Scholar4. Dirnagl U, Becker K, Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol. 2009; 8: 398– 412. CrossrefMedlineGoogle Scholar5. Ren C, Gao X, Steinberg GK, Zhao H. Limb remote-preconditioning protects against focal ischemia in rats and contradicts the dogma of therapeutic time windows for preconditioning. Neuroscience. 2008; 151: 1099– 1103. CrossrefMedlineGoogle Scholar6. Kanoria S, Jalan R, Seifalian AM, Williams R, Davidson BR. Protocols and mechanisms for remote ischemic preconditioning: a novel method for reducing ischemia reperfusion injury. Transplantation. 2007; 84: 445– 458. CrossrefMedlineGoogle Scholar7. Saxena P, Bala A, Campbell K, Meloni B, d'Udekem Y, Konstantinov IE. Does remote ischemic preconditioning prevent delayed hippocampal neuronal death following transient global cerebral ischemia in rats?Perfusion. 2009; 24: 207– 211. CrossrefMedlineGoogle Scholar8. Moskowitz MA. Brain protection: maybe yes, maybe no. Stroke. 2010; 41: S85– S86. LinkGoogle Scholar9. Tymianski M. Can molecular and cellular neuroprotection be translated into therapies for patients?: yes, but not the way we tried it before. Stroke. 41: S87–S90. LinkGoogle Scholar10. Ali ZA, Callaghan CJ, Lim E, Ali AA, Nouraei SA, Akthar AM, Boyle JR, Varty K, Kharbanda RK, Dutka DP, Gaunt ME. Remote ischemic preconditioning reduces myocardial and renal injury after elective abdominal aortic aneurysm repair: a randomized controlled trial. Circulation. 2007; 116: I98– I105. LinkGoogle Scholar11. Hoole SP, Heck PM, Sharples L, Khan SN, Duehmke R, Densem CG, Clarke SC, Shapiro LM, Schofield PM, O'Sullivan M, Dutka DP. Cardiac Remote Ischemic Preconditioning in Coronary Stenting (CRISP Stent) Study: a prospective, randomized control trial. Circulation. 2009; 119: 820– 827. LinkGoogle Scholar12. Bøtker HE, Kharbanda R, Schmidt MR, Bøttcher M, Kaltoft AK, Terkelsen CJ, Munk K, Andersen NH, Hansen TM, Trautner S, Lassen JF, Christiansen EH, Krusell LR, Kristensen SD, Thuesen L, Nielsen SS, Rehling M, Sørensen HT, Redington AN, Nielsen TT. Remote ischaemic conditioning before hospital admission, as a complement to angioplasty, and effect on myocardial salvage in patients with acute myocardial infarction: a randomised trial. Lancet. 2010; 375: 727– 734. CrossrefMedlineGoogle Scholar13. Cheung MM, Kharbanda RK, Konstantinov IE, Shimizu M, Frndova H, Li J, Holtby HM, Cox PN, Smallhorn JF, Van Arsdell GS, Redington AN. Randomized controlled trial of the effects of remote ischemic preconditioning on children undergoing cardiac surgery: first clinical application in humans. J Am Coll Cardiol. 2006; 47: 2277– 2282. CrossrefMedlineGoogle Scholar14. Zhou W, Zeng D, Chen R, Liu J, Yang G, Liu P, Zhou X. Limb ischemic preconditioning reduces heart and lung injury after an open heart operation in infants. Pediatr Cardiol. 2010; 31: 22– 29. CrossrefMedlineGoogle Scholar15. Venugopal V, Laing CM, Ludman A, Yellon DM, Hausenloy D. Effect of remote ischemic preconditioning on acute kidney injury in nondiabetic patients undergoing coronary artery bypass graft surgery: a secondary analysis of 2 small randomized trials. Am J Kidney Dis. 2010; 56: 1043– 1049. CrossrefMedlineGoogle Scholar16. Hausenloy DJ, Yellon DM. Preconditioning and postconditioning: underlying mechanisms and clinical application. Atherosclerosis. 2009; 204: 334– 341. CrossrefMedlineGoogle Scholar17. Zukin RS. Eradicating the mediators of neuronal death with a fine-tooth comb. Sci Signal. 2010; 3: pe20. CrossrefMedlineGoogle Scholar18. Stapels M, Piper C, Yang T, Li M, Stowell C, Xiong ZG, Saugstad J, Simon RP, Geromanos S, Langridge J, Lan JQ, Zhou A. Polycomb group proteins as epigenetic mediators of neuroprotection in ischemic tolerance. Sci Signal. 2010; 3: ra15. CrossrefMedlineGoogle Scholar19. Przyklenk K, Darling CE, Dickson EW, Whittaker P. Cardioprotection ‘outside the box’–the evolving paradigm of remote preconditioning. Basic Res Cardiol. 2003; 98: 149– 157. CrossrefMedlineGoogle Scholar20. Yilmaz G, Granger DN. Cell adhesion molecules and ischemic stroke. Neurol Res. 2008; 30: 783– 793. CrossrefMedlineGoogle Scholar21. Jean-St-Michel E, Manlhiot C, Li J, Tropak M, Michelsen MM, Schmidt MR, McCrindle BW, Wells GD, Redington AN. Remote preconditioning improves maximal performance in highly-trained athletes. Med Sci Sports Exerc. 2010 Dec 1. [Epub ahead of print]. Google Scholar Previous Back to top Next FiguresReferencesRelatedDetailsCited By Li Y, Huang P, Huang J, Zhong Z, Zhou S, Dong H, Xie J, Wu Y and Li P (2022) Remote ischemic preconditioning improves cognitive control in healthy adults: Evidence from an event-related potential study, Frontiers in Neuroscience, 10.3389/fnins.2022.936975, 16 Sheng R, Chen J and Qin Z (2022) Cerebral conditioning: Mechanisms and potential clinical implications, Brain Hemorrhages, 10.1016/j.hest.2021.08.003, 3:2, (62-76), Online publication date: 1-Jun-2022. Liu Y, Xu J, Zhao L, Cheng J, Chen B and Qian Y (2021) Remote Inflammatory Preconditioning Alleviates Lipopolysaccharide-Induced Acute Lung Injury via Inhibition of Intrinsic Apoptosis in Rats, Journal of Immunology Research, 10.1155/2021/1125199, 2021, (1-10), Online publication date: 20-Sep-2021. Farina M, Vieira L, Buttari B, Profumo E and Saso L (2021) The Nrf2 Pathway in Ischemic Stroke: A Review, Molecules, 10.3390/molecules26165001, 26:16, (5001) Hao Y, Xin M, Feng L, Wang X, Wang X, Ma D and Feng J (2020) Review Cerebral Ischemic Tolerance and Preconditioning: Methods, Mechanisms, Clinical Applications, and Challenges, Frontiers in Neurology, 10.3389/fneur.2020.00812, 11 Yang G, Yang Y, Li Y and Hu Z (2020) Remote liver ischaemic preconditioning protects rat brain against cerebral ischaemia–reperfusion injury by activation of an AKT‐dependent pathway, Experimental Physiology, 10.1113/EP088394, 105:5, (852-863), Online publication date: 1-May-2020. Liang W, Lin C, Yuan L, Chen L, Guo P, Li P, Wang W and Zhang X (2019) Preactivation of Notch1 in remote ischemic preconditioning reduces cerebral ischemia-reperfusion injury through crosstalk with the NF-κB pathway, Journal of Neuroinflammation, 10.1186/s12974-019-1570-9, 16:1, Online publication date: 1-Dec-2019. N T, Sangwan A, Sharma B, Majid A and GK R (2015) Cerebral Ischemic Preconditioning: the Road So Far…, Molecular Neurobiology, 10.1007/s12035-015-9278-z, 53:4, (2579-2593), Online publication date: 1-May-2016. Tülü S, Mulino M, Pinggera D, Luger M, Würtinger P, Grams A, Bodner T, Beer R, Helbok R, Matteucci-Gothe R, Unterhofer C, Gizewski E, Schmutzhard E, Thomé C and Ortler M (2015) Remote ischemic preconditioning in the prevention of ischemic brain damage during intracranial aneurysm treatment (RIPAT): study protocol for a randomized controlled trial, Trials, 10.1186/s13063-015-1102-6, 16:1, Online publication date: 1-Dec-2015. Tasker R and Duncan E (2015) Focal cerebral ischemia and neurovascular protection, Current Opinion in Pediatrics, 10.1097/MOP.0000000000000287, 27:6, (694-699), Online publication date: 1-Dec-2015. Gasparovic H, Kopjar T, Rados M, Anticevic A, Rados M, Malojcic B, Ivancan V, Fabijanic T, Cikes M, Milicic D, Gasparovic V and Biocina B (2014) Impact of remote ischemic preconditioning preceding coronary artery bypass grafting on inducing neuroprotection (RIPCAGE): study protocol for a randomized controlled trial, Trials, 10.1186/1745-6215-15-414, 15:1, Online publication date: 1-Dec-2014. Su J, Zhang T, Wang K, Zhu T and Li X (2014) Autophagy Activation Contributes to the Neuroprotection of Remote Ischemic Perconditioning Against Focal Cerebral Ischemia in Rats, Neurochemical Research, 10.1007/s11064-014-1396-x, 39:11, (2068-2077), Online publication date: 1-Nov-2014. Hamilton K, Wolfswinkel E, Weathers W, Xue A, Hatef D, Izaddoost S and Hollier L (2014) The Delay Phenomenon: A Compilation of Knowledge across Specialties, Craniomaxillofacial Trauma & Reconstruction, 10.1055/s-0034-1371355, 7:2, (112-118), Online publication date: 1-Jun-2014. Zare Mehrjerdi F, Aboutaleb N, Habibey R, Ajami M, Soleimani M, Arabian M, Niknazar S, Hossein Davoodi S and Pazoki-Toroudi H (2013) Increased phosphorylation of mTOR is involved in remote ischemic preconditioning of hippocampus in mice, Brain Research, 10.1016/j.brainres.2013.06.018, 1526, (94-101), Online publication date: 1-Aug-2013. Meybohm P, Renner J, Broch O, Caliebe D, Albrecht M, Cremer J, Haake N, Scholz J, Zacharowski K, Bein B and Biondi-Zoccai G (2013) Postoperative Neurocognitive Dysfunction in Patients Undergoing Cardiac Surgery after Remote Ischemic Preconditioning: A Double-Blind Randomized Controlled Pilot Study, PLoS ONE, 10.1371/journal.pone.0064743, 8:5, (e64743) Segev-Amzaleg N, Trudler D and Frenkel D (2013) Preconditioning to mild oxidative stress mediates astroglial neuroprotection in an IL-10-dependent manner, Brain, Behavior, and Immunity, 10.1016/j.bbi.2012.12.016, 30, (176-185), Online publication date: 1-May-2013. Simon R (2013) Tolerance, Historical Review Innate Tolerance in the CNS, 10.1007/978-1-4419-9695-4_1, (3-18), . Diane A, Pierce W, Heth C, Russell J, Richard D and Proctor S (2012) Feeding History and Obese-Prone Genotype Increase Survival of Rats Exposed to a Challenge of Food Restriction and Wheel Running, Obesity, 10.1038/oby.2011.326, 20:9, (1787-1795), Online publication date: 1-Sep-2012. February 22, 2011Vol 123, Issue 7 Advertisement Article InformationMetrics © 2011 American Heart Association, Inc.https://doi.org/10.1161/CIRCULATIONAHA.110.009688PMID: 21300956 Originally publishedFebruary 7, 2011 Keywordsacute strokebraincerebral ischemiaEditorialspostconditioningPDF download Advertisement SubjectsCardiovascular SurgeryMetabolismNeuroprotectants" @default.
• W1987282998 created "2016-06-24" @default.
• W1987282998 creator A5041862639 @default.
• W1987282998 creator A5078007632 @default.
• W1987282998 date "2011-02-22" @default.
• W1987282998 modified "2023-10-06" @default.
• W1987282998 title "Remote Ischemic Preconditioning" @default.
• W1987282998 cites W125028120 @default.
• W1987282998 cites W1966123292 @default.
• W1987282998 cites W1983038423 @default.
• W1987282998 cites W1984305956 @default.
• W1987282998 cites W2003199248 @default.
• W1987282998 cites W2016965599 @default.
• W1987282998 cites W2021949562 @default.
• W1987282998 cites W2045011381 @default.
• W1987282998 cites W2056190116 @default.
• W1987282998 cites W2063541896 @default.
• W1987282998 cites W2065348529 @default.
• W1987282998 cites W2082327290 @default.
• W1987282998 cites W2110483746 @default.
• W1987282998 cites W2122179672 @default.
• W1987282998 cites W2127508548 @default.
• W1987282998 cites W2141683458 @default.
• W1987282998 cites W2151407865 @default.
• W1987282998 cites W2162148277 @default.
• W1987282998 cites W2166660871 @default.
• W1987282998 cites W2443248231 @default.
• W1987282998 doi "https://doi.org/10.1161/circulationaha.110.009688" @default.
• W1987282998 hasPubMedId "https://pubmed.ncbi.nlm.nih.gov/21300956" @default.
• W1987282998 hasPublicationYear "2011" @default.
• W1987282998 type Work @default.
• W1987282998 sameAs 1987282998 @default.
• W1987282998 citedByCount "23" @default.
• W1987282998 countsByYear W19872829982012 @default.
• W1987282998 countsByYear W19872829982013 @default.
• W1987282998 countsByYear W19872829982014 @default.
• W1987282998 countsByYear W19872829982015 @default.
• W1987282998 countsByYear W19872829982018 @default.
• W1987282998 countsByYear W19872829982019 @default.
• W1987282998 countsByYear W19872829982020 @default.
• W1987282998 countsByYear W19872829982021 @default.
• W1987282998 countsByYear W19872829982022 @default.
• W1987282998 countsByYear W19872829982023 @default.
• W1987282998 crossrefType "journal-article" @default.
• W1987282998 hasAuthorship W1987282998A5041862639 @default.
• W1987282998 hasAuthorship W1987282998A5078007632 @default.
• W1987282998 hasBestOaLocation W19872829981 @default.
• W1987282998 hasConcept C126322002 @default.
• W1987282998 hasConcept C164705383 @default.
• W1987282998 hasConcept C2779311647 @default.
• W1987282998 hasConcept C541997718 @default.
• W1987282998 hasConcept C71924100 @default.
• W1987282998 hasConceptScore W1987282998C126322002 @default.
• W1987282998 hasConceptScore W1987282998C164705383 @default.
• W1987282998 hasConceptScore W1987282998C2779311647 @default.
• W1987282998 hasConceptScore W1987282998C541997718 @default.
• W1987282998 hasConceptScore W1987282998C71924100 @default.
• W1987282998 hasIssue "7" @default.
• W1987282998 hasLocation W19872829981 @default.
• W1987282998 hasLocation W19872829982 @default.
• W1987282998 hasOpenAccess W1987282998 @default.
• W1987282998 hasPrimaryLocation W19872829981 @default.
• W1987282998 hasRelatedWork W1890386620 @default.
• W1987282998 hasRelatedWork W2076756122 @default.
• W1987282998 hasRelatedWork W2090485917 @default.
• W1987282998 hasRelatedWork W2135004812 @default.
• W1987282998 hasRelatedWork W2350781122 @default.
• W1987282998 hasRelatedWork W2361824382 @default.
• W1987282998 hasRelatedWork W2899084033 @default.
• W1987282998 hasRelatedWork W2935909890 @default.
• W1987282998 hasRelatedWork W2778153218 @default.
• W1987282998 hasRelatedWork W3110381201 @default.
• W1987282998 hasVolume "123" @default.
• W1987282998 isParatext "false" @default.
• W1987282998 isRetracted "false" @default.
• W1987282998 magId "1987282998" @default.
• W1987282998 workType "article" @default.