Letter to the Editor: Role of subconcussion and repetitive TBI

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To The Editor: Recent publication of an article by Bailes et al.1 (Bailes JE, Petraglia AL, Omalu BI, et al: Role of subconcussion in repetitive mild traumatic brain injury. A review. J Neurosurg 119:1235–1245, November 2013) caught our eye, as we were dismayed by how they inaccurately represented parts of an article by Smith et al.10 published last year in Neurosurgery, even though we are supportive of the proof-of-concept offered.

The clinical evidence supports the concept of a subconcussion as well, and that evidence is a cornerstone of Bailes and colleagues' idea: The concept of increased neck mass and strength that may diffuse the forces imparted to the head and brain inside the skull (“slosh”) seems farfetched.

We are not convinced that it is possible to extrapolate the research of Smith et al.10 to subconcussed individuals practicing neck-strengthening exercises, all the more so as this idea was not supported by the work of Mihalik et al.7

Smith et al. conducted research on rats, and the brain injury they caused in their experiments was of a greater magnitude than that seen in the human subjects with subconcussion as reported by Bailes et al. This flaw could be highlighted even more by the argument that the model suggested by Bailes et al. was introduced by Marmarou et al.6 to induce diffuse axonal injury (DAI) in rats. DAI is on the most severe end of the traumatic axonal injury spectrum.5 The mildest end of the spectrum includes reversible axonal injury.8,11 A range of injuries that lies in the middle of the spectrum, and for which we do not know the clinical correlates, falls short of DAI in severity.2,3 On the other hand, sometimes clues in a patient's history strongly indicate that DAI was present despite a lack of evidence of hematoma or severe brain swelling on imaging studies.

By systematically studying the brains of individuals who suffered a recent documented mild head injury but died of an unrelated cause, some authors4,9 have identified scattered, hemispherically distributed traumatic axonal damage after mild head injury in patients without any noteworthy neurological or psychological symptoms.

Be that as it may, the literature suggests that extreme forces are necessary for axons to rupture soon after impact. Precisely for this reason, primary axotomy is unlikely to be present in patients who suffer concussion and have completely normal neurological function.

Disclosure

The authors report no conflict of interest.

References

  • 1.

    Bailes JEPetraglia ALOmalu BINauman ETalavage T: Role of subconcussion in repetitive mild traumatic brain injury. A review. J Neurosurg 119:123512452013

    • Search Google Scholar
    • Export Citation
  • 2.

    Blumbergs PCScott GManavis JWainwright HSimpson DAMcLean AJ: Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet 344:105510561994

    • Search Google Scholar
    • Export Citation
  • 3.

    Blumbergs PCScott GManavis JWainwright HSimpson DAMcLean AJ: Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J Neurotrauma 12:5655721995

    • Search Google Scholar
    • Export Citation
  • 4.

    Geddes JFPrimary traumatic brain injury. Whitwell HL: Forensic Neuropathology LondonEdward Arnold2005. 94106

  • 5.

    Geddes JFWhitwell HLGraham DI: Traumatic axonal injury: practical issues for diagnosis in medicolegal cases. Neuropathol Appl Neurobiol 26:1051162000

    • Search Google Scholar
    • Export Citation
  • 6.

    Marmarou AFoda MAvan den Brink WCampbell JKita HDemetriadou K: A new model of diffuse brain injury in rats. Part I: pathophysiology and biomechanics. J Neurosurg 80:2913001994

    • Search Google Scholar
    • Export Citation
  • 7.

    Mihalik JPGuskiewicz KMMarshall SWGreenwald RMBlackburn JTCantu RC: Does cervical muscle strength in youth ice hockey players affect head impact biomechanics?. Clin J Sport Med 21:4164212011

    • Search Google Scholar
    • Export Citation
  • 8.

    Miyauchi TWei EPPovlishock JT: Therapeutic targeting of the axonal and microvascular change associated with repetitive mild traumatic brain injury. J Neurotrauma 30:166416712013

    • Search Google Scholar
    • Export Citation
  • 9.

    Pfister BJIwata AMeaney DFSmith DH: Extreme stretch growth of integrated axons. J Neurosci 24:797879832004

  • 10.

    Smith DWBailes JEFisher JARobles JTurner RCMills JD: Internal jugular vein compression mitigates traumatic axonal injury in a rat model by reducing the intracranial slosh effect. Neurosurgery 70:7407462012

    • Search Google Scholar
    • Export Citation
  • 11.

    Tomei GSpagnoli DDucati ALandi AVillani RFumagalli G: Morphology and neurophysiology of focal axonal injury experimentally induced in the guinea pig optic nerve. Acta Neuropathol 80:5065131990

    • Search Google Scholar
    • Export Citation

Response

We appreciate the comments of Drs. Sosa and Stemberga concerning our article and will address their concerns over neck strengthening and the phenomenon of brain slosh. We agree that there is no scientific proof or controlled studies that demonstrate that neck strengthening is an effective strategy for reduction of brain injury or the effects of subconcussive impacts. There are several aspects, including static muscle contraction, player anticipation, gender differences, and the ability of an athlete to control sudden neck movements, that indeed make this an uncertain strategy for concussion mitigation.1 Nonetheless, some disciplines, such as in aerospace, have encouraged pilots to perform strengthening exercises for the neck to help control sudden head movements.3

We are familiar with the concepts of intracranial slosh, as the original work was performed in our laboratory.4,5 Since mild traumatic brain injury results from cranial impacts, a theory of brain slosh contends that the forces imparted to the outside of the skull cannot be interpreted without understanding how slosh dynamics translate inside the skull. In this regard, we believe that there are 2 arguments to support neck strengthening. The first is that through better tethering of the cranium, through the contraction of stronger cervical musculature on both sides, the imparted forces may be converted from rotational to less injurious linear vectors. Also, tensing, toning, or thickening the neck musculature could aid in the mere act of shortening the arc or rotational distance through which the head undergoes acceleration-deceleration. If the cranium is translated along the path of a straight line, the distance traveled is relatively less than that along an arc.

The second argument involves the potential for neck musculature strengthening to potentiate the actions of the omohyoid muscles as they impede internal jugular venous outflow. The omohyoid is an elongated, thin muscle that is directed obliquely in the anterolateral region of the neck, extending from the superior edge of the scapula to the hyoid bone. It is composed of 2 fleshy portions, the anterior and posterior bellies, separated by an intermediate tendon. One might question why teleologically there are 2 bellies, with a tendon situated directly atop the internal jugular vein (IJV). This little-understood muscle was once thought to be just an evolutionary vestige and to serve no actual purpose. However, we have postulated that the true function of this muscle may be to gently and efficiently potentiate the impedance of outflow by contracting against the IJVs, thus reducing slosh within the cranium. In doing so, the compliance of the intracranial space would thus be minimized and, like the inflating of “bubble wrap,” the brain will be better “packaged” from the inside. In the Smith et al. study, significant impact forces were imparted, and it was found that there was a marked reduction in the signature axonal injury with IJV compression.4

The contraction of the omohyoids has been shown by echographic study to cause IJV compression.2 Thus, neck strengthening and training could make the omohyoids more efficient in restricting the outflow of the IJV. The omohyoid muscle leads to a direct localized and short compression of IJV, and this in spite of possible diffuse compression by the sternocleidomastoid muscle. The latter can compress all the vascular elements of the neck it overlies, whatever the position of the head. The ability of an athlete to realize the sudden need for neck muscle contraction and the timing of such a maneuver is another matter. The above notwithstanding, the concept of neck strengthening to mitigate the forces transmitted to the human brain has not been proven and thus remains a simple suggestion for athletic training that should cause no harm, and may, in certain instances, eventually be shown to have some benefit.

References

  • 1.

    Mihalik JPGuskiewicz KMMarshall SWGreenwald RMBlackburn JTCantu RC: Does cervical muscle strength in youth ice hockey players affect head impact biomechanics?. Clin J Sport Med 21:4164212011

    • Search Google Scholar
    • Export Citation
  • 2.

    Patra PGunness TKRobert RRogez JMHeloury YLe Hur PA: Physiologic variations of the internal jugular vein surface, role of the omohyoid muscle, a preliminary echographic study. Surg Radiol Anat 10:1071121988

    • Search Google Scholar
    • Export Citation
  • 3.

    Seng KYLam PMLee VS: Acceleration effects on neck muscle strength: pilots vs. non-pilots. Aviat Space Environ Med 74:1641682003

    • Search Google Scholar
    • Export Citation
  • 4.

    Smith DWBailes JEFisher JARobles JTurner RCMills JD: Internal jugular vein compression mitigate traumatic axonal injury in rat model by reducing intracranial slosh effect. Neurosurgery 70:7407462012

    • Search Google Scholar
    • Export Citation
  • 5.

    Turner RCNaser ZJBailes JESmith DWFisher JARosen CL: Effect of slosh mitigation on histologic markers of traumatic brain injury. Laboratory investigation. J Neurosurg 117:111011182012

    • Search Google Scholar
    • Export Citation

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Article Information

Please include this information when citing this paper: published online January 17, 2014; DOI: 10.3171/2013.10.JNS132097.

© AANS, except where prohibited by US copyright law.

Headings

References

  • 1.

    Bailes JEPetraglia ALOmalu BINauman ETalavage T: Role of subconcussion in repetitive mild traumatic brain injury. A review. J Neurosurg 119:123512452013

    • Search Google Scholar
    • Export Citation
  • 2.

    Blumbergs PCScott GManavis JWainwright HSimpson DAMcLean AJ: Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet 344:105510561994

    • Search Google Scholar
    • Export Citation
  • 3.

    Blumbergs PCScott GManavis JWainwright HSimpson DAMcLean AJ: Topography of axonal injury as defined by amyloid precursor protein and the sector scoring method in mild and severe closed head injury. J Neurotrauma 12:5655721995

    • Search Google Scholar
    • Export Citation
  • 4.

    Geddes JFPrimary traumatic brain injury. Whitwell HL: Forensic Neuropathology LondonEdward Arnold2005. 94106

  • 5.

    Geddes JFWhitwell HLGraham DI: Traumatic axonal injury: practical issues for diagnosis in medicolegal cases. Neuropathol Appl Neurobiol 26:1051162000

    • Search Google Scholar
    • Export Citation
  • 6.

    Marmarou AFoda MAvan den Brink WCampbell JKita HDemetriadou K: A new model of diffuse brain injury in rats. Part I: pathophysiology and biomechanics. J Neurosurg 80:2913001994

    • Search Google Scholar
    • Export Citation
  • 7.

    Mihalik JPGuskiewicz KMMarshall SWGreenwald RMBlackburn JTCantu RC: Does cervical muscle strength in youth ice hockey players affect head impact biomechanics?. Clin J Sport Med 21:4164212011

    • Search Google Scholar
    • Export Citation
  • 8.

    Miyauchi TWei EPPovlishock JT: Therapeutic targeting of the axonal and microvascular change associated with repetitive mild traumatic brain injury. J Neurotrauma 30:166416712013

    • Search Google Scholar
    • Export Citation
  • 9.

    Pfister BJIwata AMeaney DFSmith DH: Extreme stretch growth of integrated axons. J Neurosci 24:797879832004

  • 10.

    Smith DWBailes JEFisher JARobles JTurner RCMills JD: Internal jugular vein compression mitigates traumatic axonal injury in a rat model by reducing the intracranial slosh effect. Neurosurgery 70:7407462012

    • Search Google Scholar
    • Export Citation
  • 11.

    Tomei GSpagnoli DDucati ALandi AVillani RFumagalli G: Morphology and neurophysiology of focal axonal injury experimentally induced in the guinea pig optic nerve. Acta Neuropathol 80:5065131990

    • Search Google Scholar
    • Export Citation
  • 1.

    Mihalik JPGuskiewicz KMMarshall SWGreenwald RMBlackburn JTCantu RC: Does cervical muscle strength in youth ice hockey players affect head impact biomechanics?. Clin J Sport Med 21:4164212011

    • Search Google Scholar
    • Export Citation
  • 2.

    Patra PGunness TKRobert RRogez JMHeloury YLe Hur PA: Physiologic variations of the internal jugular vein surface, role of the omohyoid muscle, a preliminary echographic study. Surg Radiol Anat 10:1071121988

    • Search Google Scholar
    • Export Citation
  • 3.

    Seng KYLam PMLee VS: Acceleration effects on neck muscle strength: pilots vs. non-pilots. Aviat Space Environ Med 74:1641682003

    • Search Google Scholar
    • Export Citation
  • 4.

    Smith DWBailes JEFisher JARobles JTurner RCMills JD: Internal jugular vein compression mitigate traumatic axonal injury in rat model by reducing intracranial slosh effect. Neurosurgery 70:7407462012

    • Search Google Scholar
    • Export Citation
  • 5.

    Turner RCNaser ZJBailes JESmith DWFisher JARosen CL: Effect of slosh mitigation on histologic markers of traumatic brain injury. Laboratory investigation. J Neurosurg 117:111011182012

    • Search Google Scholar
    • Export Citation

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