Commentaries on Viewpoint: “Tighter fit” theory—physiologists explain why “higher altitude” and jugular occlusion are unlikely to reduce risks for sports concussion and brain injuries
2017; American Physiological Society; Volume: 122; Issue: 1 Linguagem: Inglês
10.1152/japplphysiol.01022.2016
ISSN8750-7587
AutoresDamian M. Bailey, Joseph F. Clark, Gregory D. Myer, Joseph A. Fisher, Erik R. Swenson, Benjamin S. Stacey, James A. Smith, Thomas S. Owens, Damian M. Bailey,
Tópico(s)Traumatic Brain Injury and Neurovascular Disturbances
ResumoViewpointCommentaries on Viewpoint: “Tighter fit” theory—physiologists explain why “higher altitude” and jugular occlusion are unlikely to reduce risks for sports concussion and brain injuriesPublished Online:18 Jan 2017https://doi.org/10.1152/japplphysiol.01022.2016MoreSectionsPDF (53 KB)Download PDF ToolsExport citationAdd to favoritesGet permissionsTrack citations ShareShare onFacebookTwitterLinkedInWeChat FROM MONRO AND KELLIE TO MOUNTAINS AND CONCUSSION; THE SCIENCE OF SLOSHDamian M. Bailey.Author AffiliationsUniversity of South Wales, Glamorgan.University of British Columbia-Okanagan, Canada.to the editor: Protecting the brain from inside-out rather than outside-in adds a creative twist in the elusive tale of concussion prevention research popularizing altitude exposure (2) and jugular occlusion (3) as alternative interventions with the potential to promote a “tighter fit” brain and reduce slosh-induced injury. This is an adaptation of an original hypothesis developed by Ross (4) who applied the Monro-Kellie doctrine to explain the random nature of acute mountain sickness (AMS). Although I agree with Smoliga and Zavorsky (5), it is important to acknowledge that the original findings are at the very least hypothesis generating and we cannot be overly dismissive of the underlying physiological rationale. I too consider it unreasonable to attribute the lower incidence of concussions reported at such minor elevations to this mechanism, given that the hypoxic stimulus is hardly sufficient to alter craniospinal hemodynamics. Indeed, we originally questioned this mechanism even in response to far more severe hypoxia (~4,600 m), albeit within the context of AMS, although both entities share the common feature of vasogenic brain swelling. However, retrospective analysis reveals that compared with healthy controls, those prone to AMS already exhibited elevated brain to intracranial volume ratios in normoxia, a baseline difference that was almost triple the increase observed during hypoxia (1). Thus I would encourage future investigators to simply address if the “tighter fit” athlete presents with fewer postconcussive sequelae at sea level in the absence of any additional, unnecessary confounds, to add some scientific flesh to the hypothetical bones and resolve the current controversy.REFERENCES1. Kallenberg K, Bailey DM, Christ S, Mohr A, Roukens R, Menold E, Steiner T, Bärtsch P, Knauth M. Magnetic resonance imaging evidence of cytotoxic cerebral edema in acute mountain sickness. J Cereb Blood Flow Metab 27: 1064–1071, 2007. doi:10.1038/sj.jcbfm.9600404. Crossref | PubMed | ISI | Google Scholar2. Myer GD, Smith D, Barber Foss KD, Dicesare CA, Kiefer AW, Kushner AM, Thomas SM, Sucharew H, Khoury JC. Rates of concussion are lower in National Football League games played at higher altitudes. J Orthop Sports Phys Ther 44: 164–172, 2014. doi:10.2519/jospt.2014.5298. Crossref | PubMed | ISI | Google Scholar3. Myer GD, Yuan W, Barber Foss KD, Thomas S, Smith D, Leach J, Kiefer AW, Dicesare C, Adams J, Gubanich PJ, Kitchen K, Schneider DK, Braswell D, Krueger D, Altaye M. Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football. Br J Sports Med 50: 1276–1285, 2016. doi:10.1136/bjsports-2016-096134. Crossref | PubMed | ISI | Google Scholar4. Ross RT. The random nature of cerebral mountain sickness. Lancet 1: 990–991, 1985. doi:10.1016/S0140-6736(85)91771-4. Crossref | PubMed | ISI | Google Scholar5. Smoliga JM, Zavorsky GS. “Tighter fit” theory - physiologists explain why “higher altitude” and jugular occlusion are unlikely to reduce risks for sports concussion and brain injuries. J Appl Physiol (1985). doi:10.1152/japplphysiol.00661.2016. Link | ISI | Google ScholarREFERENCES1. Kallenberg K, Bailey DM, Christ S, Mohr A, Roukens R, Menold E, Steiner T, Bärtsch P, Knauth M. Magnetic resonance imaging evidence of cytotoxic cerebral edema in acute mountain sickness. J Cereb Blood Flow Metab 27: 1064–1071, 2007. doi:10.1038/sj.jcbfm.9600404. Crossref | PubMed | ISI | Google Scholar2. Myer GD, Smith D, Barber Foss KD, Dicesare CA, Kiefer AW, Kushner AM, Thomas SM, Sucharew H, Khoury JC. Rates of concussion are lower in National Football League games played at higher altitudes. J Orthop Sports Phys Ther 44: 164–172, 2014. doi:10.2519/jospt.2014.5298. Crossref | PubMed | ISI | Google Scholar3. Myer GD, Yuan W, Barber Foss KD, Thomas S, Smith D, Leach J, Kiefer AW, Dicesare C, Adams J, Gubanich PJ, Kitchen K, Schneider DK, Braswell D, Krueger D, Altaye M. Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football. Br J Sports Med 50: 1276–1285, 2016. doi:10.1136/bjsports-2016-096134. Crossref | PubMed | ISI | Google Scholar4. Ross RT. The random nature of cerebral mountain sickness. Lancet 1: 990–991, 1985. doi:10.1016/S0140-6736(85)91771-4. Crossref | PubMed | ISI | Google Scholar5. Smoliga JM, Zavorsky GS. “Tighter fit” theory - physiologists explain why “higher altitude” and jugular occlusion are unlikely to reduce risks for sports concussion and brain injuries. J Appl Physiol (1985). doi:10.1152/japplphysiol.00661.2016. Link | ISI | Google ScholarEXPLANATION OF BRAIN PHYSIOLOGY TO ENHANCE UNDERSTANDING OF THE “TIGHTER FIT” THEORYJoseph F. Clark.Author AffiliationsUniversity of Cincinnati.Gregory D. Myer.Author AffiliationsUniversity of Cincinnati.University of Pennsylvania.to the editor: Smoliga and Zavorsky (3) criticize rodent studies demonstrating neuroprotection with jugular vein compression. They claim the forces used (900 g) are excessive compared with forces causing human concussions (100 g). Two points of clarification, the forces used in rodents to ensure validity are of that magnitude, and the investigation in question demonstrated benefits.The authors say, “mild jugular compression may alter selected cephalic blood flow and CSF parameters at some points within the cardiac cycle.” This incorrectly implies that venous sinuous drainage depends on the cardiac cycle. The sinuses engorge when intrathoracic pressures are increased. This physiology is taught in combat sports and has been demonstrated in clinical trials to mimic the collar effect with Valsalva-like maneuvers (2).Contraction of the omo-hyoid muscle modulates jugular outflow. Reducing the outflow by a small amount can quickly provide 3–5 ml of intracranial blood with concomitant compliance changes. As the densities of the intracranial contents are heterogeneous, repackaging the brain allows the brain’s contents to move in unison when exposed to concussive forces. This could provide a physiological mechanism to maintain a “tighter fit” of intracranial packaging while simultaneously protecting the brain.The authors support their position by referencing their flawed meta-analysis (5). The corrected meta-analysis shows errors undermining their thesis (1). As “science is distinguished from pseudoscience when the same phenomenon is sought by independent investigation” (4), we encourage Smoliga and Zavorsky to move away from tangential studies of and direct their attention to the analysis of data from replicated preclinical and clinical trials.REFERENCES1. Myer GD, Schneider DK, Khoury J. Risk of concussion for athletes in contact sports at higher altitude vs at sea level: a meta-analysis–corrected. [Epub ahead of print] JAMA Neurol, in press.Google Scholar2. Myer GD, Yuan W, Barber Foss KD, Thomas S, Smith D, Leach J, Kiefer AW, Dicesare C, Adams J, Gubanich PJ, Kitchen K, Schneider DK, Braswell D, Krueger D, Altaye M. Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football. Br J Sports Med 50: 1276–1285, 2016. doi:10.1136/bjsports-2016-096134. Crossref | PubMed | ISI | Google Scholar3. Smoliga JM, Zavorsky GS. “Tighter fit” theory - physiologists explain why “higher altitude” and jugular occlusion are unlikely to reduce risks for sports concussion and brain injuries. J Appl Physiol (1985). doi:10.1152/japplphysiol.00661.2016. Link | ISI | Google Scholar4. Wilson EO. Consilience: The Unity of Knowledge, 1st ed. New York: Knopf, 1998.Google Scholar5. Zavorsky GS, Smoliga JM. Risk of concussion for athletes in contact sports at higher altitude vs at sea level: a meta-analysis. JAMA Neurol 73: 1369–1370, 2016. doi:10.1001/jamaneurol.2016.0795. Crossref | PubMed | ISI | Google ScholarREFERENCES1. Myer GD, Schneider DK, Khoury J. Risk of concussion for athletes in contact sports at higher altitude vs at sea level: a meta-analysis–corrected. [Epub ahead of print] JAMA Neurol, in press.Google Scholar2. Myer GD, Yuan W, Barber Foss KD, Thomas S, Smith D, Leach J, Kiefer AW, Dicesare C, Adams J, Gubanich PJ, Kitchen K, Schneider DK, Braswell D, Krueger D, Altaye M. Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football. Br J Sports Med 50: 1276–1285, 2016. doi:10.1136/bjsports-2016-096134. Crossref | PubMed | ISI | Google Scholar3. Smoliga JM, Zavorsky GS. “Tighter fit” theory - physiologists explain why “higher altitude” and jugular occlusion are unlikely to reduce risks for sports concussion and brain injuries. J Appl Physiol (1985). doi:10.1152/japplphysiol.00661.2016. Link | ISI | Google Scholar4. Wilson EO. Consilience: The Unity of Knowledge, 1st ed. New York: Knopf, 1998.Google Scholar5. Zavorsky GS, Smoliga JM. Risk of concussion for athletes in contact sports at higher altitude vs at sea level: a meta-analysis. JAMA Neurol 73: 1369–1370, 2016. doi:10.1001/jamaneurol.2016.0795. Crossref | PubMed | ISI | Google ScholarCOMMENTARY ON VIEWPOINT: “TIGHTER FIT” THEORY—PHYSIOLOGISTS EXPLAIN WHY “HIGHER ALTITUDE” AND JUGULAR OCCLUSION ARE UNLIKELY TO REDUCE RISKS FOR SPORTS CONCUSSION AND BRAIN INJURIESJoseph A. Fisher.Author AffiliationsUniversity of Toronto, Canada.to the editor: As one of the early adopters of slosh theory and developers of the collar approach, I thank you for the opportunity to address the Viewpoint paper on the tight fit hypothesis and concussion by Smoliga and Zavorsky (5). Leaving aside their skepticism regarding the effect of altitude on concussion, I will briefly address some of their other objections to slosh theory. First, although intracranial volume (ICV) does ordinarily depend on cardiac cycle and posture as claimed, subocclusive internal jugular vein pressure enables a minimum ICV independent of them. Second, it seems inappropriate to dismiss the data from the jugular occlusion study in rats because they suffered 8× the brain acceleration typical in football, because this level of acceleration is part of the rat concussion model and was applied to both test and control subjects. If anything, this demonstrates the magnitude of the protective effect. Third, the authors cite simulated necktie studies (3) that show reductions in cerebrovascular reactivity as evidence of potential—not actual—harm. But, a pneumatic tube around the neck inflated to 60 mmHg does not simulate subocclusive internal jugular vein pressure. Even so, the cerebrovascular reactivity in their cited studies remained within the normal range. Finally, I believe that hard data (1, 2, 4) should not be challenged by appealing to authority, i.e., being physiologists, or by expressing skepticism (supported by tenuously related citations, I might add) about the proffered explanation for the data—but by providing alternative hard data.REFERENCES1. Myer GD, Yuan W, Barber Foss KD, Smith D, Altaye M, Reches A, Leach J, Kiefer AW, Khoury JC, Weiss M, Thomas S, Dicesare C, Adams J, Gubanich PJ, Geva A, Clark JF, Meehan WP III, Mihalik JP, Krueger D. The effects of external jugular compression applied during head impact exposure on longitudinal changes in brain neuroanatomical and neurophysiological biomarkers: A preliminary investigation. Front Neurol 7: 74, 2016. doi:10.3389/fneur.2016.00074. Crossref | PubMed | ISI | Google Scholar2. Myer GD, Yuan W, Barber Foss KD, Thomas S, Smith D, Leach J, Kiefer AW, Dicesare C, Adams J, Gubanich PJ, Kitchen K, Schneider DK, Braswell D, Krueger D, Altaye M. Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football. Br J Sports Med 50: 1276–1285, 2016. doi:10.1136/bjsports-2016-096134. Crossref | PubMed | ISI | Google Scholar3. Rafferty M, Quinn TJ, Dawson J, Walters M. Neckties and cerebrovascular reactivity in young healthy males: a pilot randomised crossover trial. Stroke Res Treat 2011: 692595, 2010. doi:10.4061/2011/692595. Crossref | PubMed | Google Scholar4. Smith DW, Bailes JE, Fisher JA, Robles J, Turner RC, Mills JD. Internal jugular vein compression mitigates traumatic axonal injury in a rat model by reducing the intracranial slosh effect. Neurosurgery 70: 740–746, 2012. doi:10.1227/NEU.0b013e318235b991. Crossref | PubMed | ISI | Google Scholar5. Smoliga JM, Zavorsky GS. “Tighter fit” theory - physiologists explain why “higher altitude” and ` sports concussion and brain injuries. J Appl Physiol (1985). doi:10.1152/japplphysiol.00661.2016. Link | ISI | Google ScholarREFERENCES1. Myer GD, Yuan W, Barber Foss KD, Smith D, Altaye M, Reches A, Leach J, Kiefer AW, Khoury JC, Weiss M, Thomas S, Dicesare C, Adams J, Gubanich PJ, Geva A, Clark JF, Meehan WP III, Mihalik JP, Krueger D. The effects of external jugular compression applied during head impact exposure on longitudinal changes in brain neuroanatomical and neurophysiological biomarkers: A preliminary investigation. Front Neurol 7: 74, 2016. doi:10.3389/fneur.2016.00074. Crossref | PubMed | ISI | Google Scholar2. Myer GD, Yuan W, Barber Foss KD, Thomas S, Smith D, Leach J, Kiefer AW, Dicesare C, Adams J, Gubanich PJ, Kitchen K, Schneider DK, Braswell D, Krueger D, Altaye M. Analysis of head impact exposure and brain microstructure response in a season-long application of a jugular vein compression collar: a prospective, neuroimaging investigation in American football. Br J Sports Med 50: 1276–1285, 2016. doi:10.1136/bjsports-2016-096134. Crossref | PubMed | ISI | Google Scholar3. Rafferty M, Quinn TJ, Dawson J, Walters M. Neckties and cerebrovascular reactivity in young healthy males: a pilot randomised crossover trial. Stroke Res Treat 2011: 692595, 2010. doi:10.4061/2011/692595. Crossref | PubMed | Google Scholar4. Smith DW, Bailes JE, Fisher JA, Robles J, Turner RC, Mills JD. Internal jugular vein compression mitigates traumatic axonal injury in a rat model by reducing the intracranial slosh effect. Neurosurgery 70: 740–746, 2012. doi:10.1227/NEU.0b013e318235b991. Crossref | PubMed | ISI | Google Scholar5. Smoliga JM, Zavorsky GS. “Tighter fit” theory - physiologists explain why “higher altitude” and ` sports concussion and brain injuries. J Appl Physiol (1985). doi:10.1152/japplphysiol.00661.2016. Link | ISI | Google ScholarCOMMENTARY ON VIEWPOINT: “TIGHTER FIT” THEORY—PHYSIOLOGISTS EXPLAIN WHY “HIGHER ALTITUDE” AND JUGULAR OCCLUSION ARE UNLIKELY TO REDUCE RISKS FOR SPORTS CONCUSSION AND BRAIN INJURIESErik R. Swenson.Author AffiliationsUniversity of Washington.to the editor: I concur with the concerns raised by Smoliga and Zavorsky (6) about inappropriate altitude classifications and assuming that the associated hypoxia explains the particular phenomena observed. This problem afflicts studies reporting health benefits of living at altitude. For example, de Leon et al. (1) found correlations between altitude and hemodynamic/metabolic parameters in 1,000 Canary Islanders, but with only 10% living above 600 m. They reported residence above 200 m favorably alters heart rate and inflammatory biomarkers and speculated these explain lower mortality in higher altitude populations as observed by Winkelmayer and Faeh and colleagues (3, 8). In over 2.4 million people, there was no correlation of altitude with mortality below 1,200 m.The PIO2reduction at 600 m (1,800 ft) from 149 to 137 mmHg is trivial. Lowlanders spending 5 days in a normobaric chamber at a PIO2of 138 mmHg have no arterial Pco2 decrease or change in ventilation (2). Furthermore, populations living below 1,600 m have equal hematocrits to those at sea level (7), consistent with data that erythropoietin release requires inspired oxygen fall to Volume 122Issue 1January 2017Pages 218-220 Copyright & PermissionsCopyright © 2017 the American Physiological Societyhttps://doi.org/10.1152/japplphysiol.01022.2016PubMed28100448History Received 14 November 2016 Accepted 14 November 2016 Published online 18 January 2017 Published in print 1 January 2017 Metrics
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