Letter to the Editor. Glasgow Coma Scale–Pupils Score: opening the eyes to new ways of predicting outcomes in TBI

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TO THE EDITOR: We have read with great attention the articles by Brennan et al.1 and Murray et al.4 (Brennan PM, Murray GD, Teasdale GM: Simplifying the use of prognostic information in traumatic brain injury. Part 1: The GCS-Pupils score: an extended index of clinical severity. J Neurosurg 128:1612–1620, June 2018; Murray GD, Brennan PM, Teasdale GM: Simplifying the use of prognostic information in traumatic brain injury. Part 2: Graphical presentation of probabilities. J Neurosurg 128:1621–1634, June 2018). First, we would like to congratulate the authors. These are indeed fascinating papers on traumatic brain injury (TBI). We agree with many of their statements.3,4

The authors performed a study analyzing available data from 9045 and 6855 patients, respectively, from the CRASH (Corticosteroid Randomisation After Significant Head Injury) and IMPACT (International Mission for Prognosis and Clinical Trials in TBI) clinical trials. Information such as Glasgow Coma Scale (GCS) score, pupil response, patient age, CT findings, and Glasgow Outcome Scale (GOS) score were combined into a pooled data set for the main analysis.1,3,5,6

However, we think some analytical issues are worth discussing. First, over the years, more than 100 methods have been tried to make outcome predictions in TBI. The challenge is to transform simple measurements into information for clinical practice. The authors performed an excellent analysis of a large data set, associating the relationship of the GCS-Pupils (GCS-P) score with mortality. They showed an association between a patient’s loss of pupil reactivity and a worse outcome. Compared to methods that use other variables, the pupillary response is simpler to evaluate with quite reproducible results.3,7,8 However, the type of pupil response may compromise method applicability. Patient sedation is a factor because it may alter the pupilar response.

Theirs was a retrospective study based on two large and heterogeneous trials. We believe that although the statistical evaluation is adequate, it may harbor bias because of free data and different protocol evaluations and populations. A prospective study may be an alternative to these problems, although they are long and expensive.

The loss of pupil reactivity was more common in patients with GCS scores at or below 8 (35.7%) than in the patients with GCS scores 13 and higher (2.1%), precisely the subgroup that needs information on mortality. Therefore, there is a differential loss, which causes bias and may impact the final results. Conversely, as acknowledged by the authors, patients with a GCS-P score of 4 had higher rates of mortality and unfavorable outcomes than individuals with a GCS-P score of 3. Additionally, a GCS-P score of 1 or 2 slightly underestimated the likelihood of an adverse outcome. These facts may be related to selection bias in the original trials.

Nonetheless, when it comes to consciousness level scales, a pertinent question is whether we should test more or less. The Simplified Motor Score (SMS)2 is an interesting alternative to the GCS that has been proven to be a good predictor of outcome. The verbal response may sometimes be misleading, as focal verbal deficit lowers the score on the GCS without any impairment in consciousness level. It would be interesting to see how the GCS-P performs compared to the SMS.

The critical point is to use the adequate score in clinical practice to predict mortality in brain injury. The GCS-P seems to be a useful tool but needs further investigation to compare it with existing scales and apply it in clinical practice. The inclusion of pupillary response in the GCS is a thoughtful refinement, as we all know the strong clinical meaning of anisocoria or fixed, dilated pupils.8,9

Disclosures

The authors report no conflict of interest.

References

  • 1

    Brennan PMMurray GDTeasdale GM: Simplifying the use of prognostic information in traumatic brain injury. Part 1: The GCS-Pupils score: an extended index of clinical severity. J Neurosurg 128:161216202018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Haukoos JSGill MRRabon REGravitz CSGreen SM: Validation of the Simplified Motor Score for the prediction of brain injury outcomes after trauma. Ann Emerg Med 50:18242007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Junior JRWelling LCSchafranski MYeng LTdo Prado RRKoterba E: Prognostic model for patients with traumatic brain injuries and abnormal computed tomography scans. J Clin Neurosci 42:1221282017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Murray GDBrennan PMTeasdale GM: Simplifying the use of prognostic information in traumatic brain injury. Part 2: Graphical presentation of probabilities. J Neurosurg 128:162116342018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Nell VYates DWKruger J: An extended Glasgow Coma Scale (GCS-E) with enhanced sensitivity to mild brain injury. Arch Phys Med Rehabil 81:6146172000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Osler TCook AGlance LGLecky FBouamra OGarrett M: The differential mortality of Glasgow Coma Score in patients with and without head injury. Injury 47:187918852016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Silverberg NDGardner AJBrubacher JRPanenka WJLi JJIverson GL: Systematic review of multivariable prognostic models for mild traumatic brain injury. J Neurotrauma 32:5175262015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Steyerberg EWMushkudiani NPerel PButcher ILu JMcHugh GS: Predicting outcome after traumatic brain injury: development and international validation of prognostic scores based on admission characteristics. PLoS Med 5:e1652008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Teasdale GMaas ALecky FManley GStocchetti NMurray G: The Glasgow Coma Scale at 40 years: standing the test of time. Lancet Neurol 13:8448542014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

INCLUDE WHEN CITING Published online May 24, 2019; DOI: 10.3171/2019.2.JNS19358.

Response

We are grateful to the authors for their supportive comments on our development of a simple tool that combines the GCS and pupil reactivity data to provide a clinical index of the early severity of TBI. We wish to reassure them that their concerns about “bias” are unnecessary. The data used in our analysis were collected prospectively, not retrospectively as they assert, and it is precisely the large size and heterogeneous nature of the data that makes the results so likely to be widely applicable. Moreover, although the loss of pupil reactivity was more frequent in patients with more severe head injuries—unsurprisingly, given the physiological mechanism by which it arises—we demonstrated that the adverse effect of the loss of pupil reactivity was not restricted to such patients. Instead, it applied across the spectrum of GCS scores from 3 to 15 (Fig. 2 in Brennan et al.) and thus was not subject to bias from the composition of the series.

We report that the pupil reactivity score, derived by subtracting 1 or 2 from the GCS score according to the number of nonreactive pupils, was developed to be simple and that it slightly underestimates the likelihood of poor outcomes at lower GCS scores. This is also not bias from the data, but rather a choice of modeling for clinical utility, informed by statistical analysis.

In the studies from which the data in our analysis were taken (CRASH and IMPACT), pupil reactivity was assessed as a simple pupil response to light. No caveats are described as to how to interpret this simple assessment. When the patient has self-administered or been given drugs that affect pupil reactivity, it will not be possible to make the full assessment necessary to determine the GCS-P score. Similarly, the apparent lower mortality with a GCS score of 3 versus 4 is likely to result from allocating a score to patients whose responsiveness was depressed pharmacologically (“pseudothrees”’), and the smoothing out of the relationship is a further advantage of the GCS-P score.2

Like the authors, we would welcome assessment of the GCS-P and the associated GCS-PA chart (GCS-P plus age) in other large, relevant neurotrauma data sets and against other systems for the assessment of TBI severity. However, we do not expect the shortened scales to match the discrimination in stratifying patients for early severity, for monitoring changes in the individual, or in relating to prognosis for different late outcomes provided by the 15-point GCS-P. The SMS the authors refer to was actually developed for use by technicians in making binary decisions in prehospital care, and extensive studies have already shown that it has no benefit over the basic GCS in predicting early mortality.1,3 We do agree with Nícollas Rabelo and his colleagues that there is a need to strike a balance between simplification and complexity in estimating a patient’s likely outcome. We believe that the combination of clinical, demographic, and imaging information in the GCS-PA charts3 provides this in a way that will be easy to understand and use in clinical practice.

References

  • 1

    Chou RTotten AMCarney NDandy SFu RGrusing S: Predictive utility of the total Glasgow Coma Scale versus the motor component of the Glasgow Coma Scale for identification of patients with serious traumatic injuries. Ann Emerg Med 70:143157157.e1–157.e6 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Osler TCook AGlance LGLecky FBouamra OGarrett M: The differential mortality of Glasgow Coma Score in patients with and without head injury. Injury 47:187918852016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Singh BMurad MHProkop LJErwin PJWang ZMommer SK: Meta-analysis of Glasgow Coma Scale and Simplified Motor Score in predicting traumatic brain injury outcomes. Brain Inj 27:2933002013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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Article Information

Correspondence Eberval Gadelha Figueiredo: ebgadelha@yahoo.com.

INCLUDE WHEN CITING Published online May 24, 2019; DOI: 10.3171/2019.2.JNS19296.

Disclosures The authors report no conflict of interest.

© AANS, except where prohibited by US copyright law.

Headings

References

  • 1

    Brennan PMMurray GDTeasdale GM: Simplifying the use of prognostic information in traumatic brain injury. Part 1: The GCS-Pupils score: an extended index of clinical severity. J Neurosurg 128:161216202018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Haukoos JSGill MRRabon REGravitz CSGreen SM: Validation of the Simplified Motor Score for the prediction of brain injury outcomes after trauma. Ann Emerg Med 50:18242007

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Junior JRWelling LCSchafranski MYeng LTdo Prado RRKoterba E: Prognostic model for patients with traumatic brain injuries and abnormal computed tomography scans. J Clin Neurosci 42:1221282017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Murray GDBrennan PMTeasdale GM: Simplifying the use of prognostic information in traumatic brain injury. Part 2: Graphical presentation of probabilities. J Neurosurg 128:162116342018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Nell VYates DWKruger J: An extended Glasgow Coma Scale (GCS-E) with enhanced sensitivity to mild brain injury. Arch Phys Med Rehabil 81:6146172000

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Osler TCook AGlance LGLecky FBouamra OGarrett M: The differential mortality of Glasgow Coma Score in patients with and without head injury. Injury 47:187918852016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    Silverberg NDGardner AJBrubacher JRPanenka WJLi JJIverson GL: Systematic review of multivariable prognostic models for mild traumatic brain injury. J Neurotrauma 32:5175262015

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Steyerberg EWMushkudiani NPerel PButcher ILu JMcHugh GS: Predicting outcome after traumatic brain injury: development and international validation of prognostic scores based on admission characteristics. PLoS Med 5:e1652008

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Teasdale GMaas ALecky FManley GStocchetti NMurray G: The Glasgow Coma Scale at 40 years: standing the test of time. Lancet Neurol 13:8448542014

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 1

    Chou RTotten AMCarney NDandy SFu RGrusing S: Predictive utility of the total Glasgow Coma Scale versus the motor component of the Glasgow Coma Scale for identification of patients with serious traumatic injuries. Ann Emerg Med 70:143157157.e1–157.e6 2017

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Osler TCook AGlance LGLecky FBouamra OGarrett M: The differential mortality of Glasgow Coma Score in patients with and without head injury. Injury 47:187918852016

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Singh BMurad MHProkop LJErwin PJWang ZMommer SK: Meta-analysis of Glasgow Coma Scale and Simplified Motor Score in predicting traumatic brain injury outcomes. Brain Inj 27:2933002013

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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