Clinical examination for prognostication (ALS): Systematic Review

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This Review is a draft version prepared by ILCOR, with the purpose to allow the public to comment and is labeled “Draft for Public Comment". The comments will be considered by ILCOR. The next version will be labelled “draft" to comply with copyright rules of journals. The final Review will be published on this website once a summary article has been published in a scientific Journal and labeled as “final”.

Conflict of Interest Declaration

The ILCOR Continuous Evidence Evaluation process is guided by a rigorous ILCOR Conflict of Interest policy. The following Task Force members and other authors were recused from the discussion as they declared a conflict of interest: none applicable

The following Task Force members and other authors declared an intellectual conflict of interest and this was acknowledged and managed by the Task Force Chairs and Conflict of Interest committees: Tobias Cronberg and Claudio Sandroni are co-authors of some of the included studies in the present review. They were excluded from the bias assessment of these studies.

CoSTR Citation

Sandroni C, Cacciola S, Cronberg T, D’Arrigo S, Hoedemaekers CWE, Kamps M, Nolan JP, Böttiger BW, Andersen LW , Callaway CW, Deakin CD, Donnino MW, Drennan I, Hsu C, Morley PM, Nicholson TC, O’Neil BJ, Neumar RW, Paiva EF, Parr MJ, Reynolds JC, Wang TL, Welsford M, Berg KM, Soar J. Clinical examination for prognostication. Consensus on Science with Treatment Recommendations [Internet] Brussels, Belgium: International Liaison Committee on Resuscitation (ILCOR) Advanced Life Support Task Force, 2020 Jan 1. Available from: http://ilcor.org.

Methodological preamble

The continuous evidence evaluation process for the production of Consensus on Science with Treatment Recommendations (CoSTR) started with a systematic review of prognostication after cardiac arrest (Sandroni C 2020 – PROSPERO: CRD 420 1914 1169) conducted by a systematic review team with involvement of clinical content experts from the ILCOR ALS Task Force.

Systematic review

Sandroni C et al. Clinical examination for prognostication in comatose survivors of cardiac arrest. In preparation .

PICOST

The PICOST (Population, Intervention, Comparator, Outcome, Study Designs and Timeframe)

Population: Adults who are comatose after resuscitation from cardiac arrest (either in-hospital or out-of-hospital), regardless of target temperature.

Intervention: Pupillary light reflex (PLR), Pupillometry, Corneal Reflex (CR), Myoclonus and Status Myoclonus, assessed within one week from cardiac arrest.

Comparator: none.

Outcome: Prediction of poor neurological outcome defined as Cerebral Performance Categories (CPC) 3-5 or modified Rankin Score (mRS) 4-6 at hospital discharge/1 month or later.

Study Design: Prognostic accuracy studies where the 2 x 2 contingency table (i.e., the number of true/false negatives and positives for prediction of poor outcome) was reported, or where those variables could be calculated from reported data, are eligible for inclusion. Unpublished studies, reviews, case reports, case series, studies including less than 10 patients, letters, editorials, conference abstracts, and studies published in abstract form were excluded.

Timeframe: In 2015, an ILCOR evidence review identified four categories of predictors of neurological outcome after cardiac arrest, namely clinical examination, biomarkers, electrophysiology and imaging. In the last four years, several studies have been published and new predictors have been identified, therefore the topic needs an update.

The most recent search of the previous systematic reviews on neuroprognostication was launched on May 31, 2013. We searched studies published from January 1, 2013 onwards.

PROSPERO: CRD 420 1914 1169

Consensus on science

Pupillary reflex

A bilaterally absent standard pupillary light reflex was investigated in twenty-four observational studies [Choi 2017 70; Chung-Esaki 2018 99; Kim 2013 57; Ryoo 2015 2370; Javaudin 2018 8; Sivaraju 2015 1264; Scarpino 2019 in press; Dhakal 2016 116; Matthews 2018 66; Oddo 2018 2102; Fatuzzo 2018 29; Tsetsou 2018 104; Dragancea 2015 164; Solari 2017 804; Rossetti 2017 e674; Hofmeijer 2015 137; Kongpolprom 2018 509; Roger 2015 231; Zhou 2019 343; Greer 2013 (a) 1546; Greer 2013 (b) 899; Ruijter 2015 1845; Kim 2018 33; Lee 2017 1628].

In four studies [Choi 2017 70, 115 pts; Kim 2013 57, 51 pts; Ryoo 2015 2370, 172 pts; Javaudin 2018 8, 10151 pts] absent standard pupillary light reflex immediately after ROSC predicted poor neurologic outcome at hospital discharge or 1 month with specificity ranging from 47.6% to 75.9% and sensitivity ranging from 65.5% to 86.7% (very-low certainty of evidence).

In five studies [Sivaraju 2015 1264, 97 pts; Scarpino 2019 in press, 336 pts; Dhakal 2016 116, 99 pts; Matthews 2018 66, 392 pts; Oddo 2018 2102, 137 pts] absent standard pupillary light reflex at ≤24h predicted poor neurologic outcome from hospital discharge to 12 months with specificity ranging from 80% to 92.3% and sensitivity ranging from 26.5% to 63.2 % (very-low certainty of evidence).

In three studies [Fatuzzo 2018 29, 490 pts; Dragancea 2015 164, 36 pts; Solari 2017 804, 99 pts] absent standard pupillary light reflex at 36-72h predicted poor neurologic outcome from 3 months to 12 months with specificity ranging from 95.8% to 100% and sensitivity ranging from 36.5% to 48.4% (very-low certainty of evidence).

In five studies [Oddo 2018 2102, 279 pts; Hofmeijer 2015 137, 272 pts; Sivaraju 2015 1264, 83 pts; Kongolprom 2018 509, 51 pts; Roger 2015 231, 61 pts] absent standard pupillary light reflex 48-72h predicted poor neurologic outcome from hospital discharge to 6 months with specificity ranging from 89.7% to 100% and sensitivity ranging from 17.8% to 58.2% (very-low certainty of evidence).

In eight studies [Dhakal 2016 116, 98 pts; Greer 2013 (a) 1546, 104 pts; Greer 2013 (b) 899, 80 pts; Chung-Esaki 2018 99, 90 pts; Ruijter 2015 1845, 47 pts; Matthews 2018 66, 137 pts] absent standard pupillary light reflex at 72h predicted poor neurologic outcome from hospital discharge to 12 months with specificity ranging from 93.6% to 100% and sensitivity ranging from 10.8% to 29.2% (very-low certainty of evidence).

In seven studies [Dragancea 2015 164, 78 pts; Kim 2018 33, 192 pts; Lee 2017 1628, 53 pts; Zhou 2019 343, 189 pts; Matthews 2018 66, 137 pts; Kongolprom 2018 509, 51 pts; Greer 2013 (a) 1546, 59 pts] absent standard pupillary light reflex from 72h to day 7 predicted poor neurologic outcome from hospital discharge to 12 months with specificity ranging from 92.3% to 100% and sensitivity ranging from 17.9% to 63.1% (very-low certainty of evidence).

Pupillometry

Automated assessment of pupillary reflex to light (PLR) has been made by measuring two variables:

  • The percentage of reduction in pupillary size, reported as qPLR
  • The neurological pupil index (NPi), based on several variables, such as pupillary size, percentage of constriction, constriction velocity and latency.

AUTOMATED PUPILLOMETRY: qPLR

Quantitative pupillary light reflex was investigated in three observational studies [Oddo 2018 2102; Heimburger 2016 88; Solari 2017 804].

In three studies [Oddo 2018 2102, 434 pts; Heimburger 2016 88, 82 pts; Solari 2017 804, 101 pts] qPLR from 0% to 13% at 24h predicted poor neurological outcome from 3 months to 12 months with specificity ranging from 77.8% to 98.9% and sensitivity ranging from 17% to 66% (certainty of evidence from moderate to very low).

In three studies [Oddo 2018 2102, 356 pts; Heimburger 2016 88, 82 pts; Solari 2017 804, 101 pts] qPLR from 0% to 13% at 48h predicted poor neurological outcome from 3 months to 12 months with specificity ranging from 95.7% to 100% and sensitivity ranging from 18.1% to 58.5% (certainty of evidence from low to very low).

In one study [Oddo 2018 2102, 234 pts] qPLR=0% at 72h predicted poor neurological outcome at 3 months with 100% specificity and 4.9% sensitivity (moderate certainty of evidence).

AUTOMATED PUPILLOMETRY: NPi

NPi was investigated in three observational studies [Riker 2019 in press; Obling 2019 in press; Oddo 2018 2102].

In three studies [Riker 2019 in press, 52 pts; Obling 2019 in press, 127 pts; Oddo 2018 2102, 450 pts] NPi from 0 to 2.40 within 24h predicted poor neurological outcome from hospital discharge to 3 months with 100% specificity and sensitivity ranging from 22% to 43.9% (certainty of evidence from low to very low).

In one study [Oddo 2018 2102, 361 pts] NPi≤2 at 48h predicted poor neurological outcome at 3 months with 100% specificity and 18.8% sensitivity (moderate certainty of evidence).

In one study [Oddo 2018 2102, 271 pts] NPi≤2 at 72h predicted poor neurological outcome at 3 months with 100% specificity and 16.9% sensitivity (moderate certainty of evidence).

Corneal reflex

CR was investigated in fourteen observational studies [Choi 2017 70; Chung-Esaki 2018 99; Kim 2013 134; Ryoo 2015 2370; Sivaraju 2015 1264; Matthews 2018 66; Fatuzzo 2018 29; Dragancea 2015 164; Solari 2017 804; Kongpolprom 2018 509; Zhou 2019 343; Greer 2013 (a) 1546; Greer 2013 (b) 899; Kim 2018 57].

In three studies [Choi 2017 70, 115 pts; Kim 2013 134, 51 pts; Ryoo 2015 2370, 172 pts;] absent corneal reflex immediately after ROSC predicted poor neurological outcome at hospital discharge with specificity ranging from 25.8% to 50% and sensitivity ranging from 93.2% to 96.4% (very-low certainty of evidence).

In two studies [Sivaraju 2015 1264, 97 pts; Matthews 2018 66, 137 pts;] absent corneal reflex at ≤24h predicted poor neurologic outcome from hospital discharge to 12 months with specificity ranging from 58.6% to 65.7% and sensitivity ranging from 51% to 79.4% (very-low certainty of evidence).

In five studies [Fatuzzo 2018 29, 490 pts; Sivaraju 2015 1264, 83 pts; Kongpolprom 2018 509, 51 pts; Dragancea 2015 164, 33 pts; Solari 2017 804, 99 pts] absent corneal reflex at 36-72h predicted poor neurologic outcome from hospital discharge to 12 months with specificity ranging from 88.9% to 100% and sensitivity ranging from 33.3% to 67.3% (very-low certainty of evidence).

In four studies [Chung-Esaki 2018 99, 85 pts; Greer 2013 (a) 1546, 104 pts; Greer 2013 (b) 899, 80 pts; Matthews 2018 66, 137 pts] absent corneal reflex at 72h predicted poor neurologic outcome from hospital discharge to 12 months with specificity ranging from 94.3% to 100% and sensitivity ranging from 32.4% to 48.8% (very-low certainty of evidence).

In five studies [Dragancea 2015 164, 127 pts; Kim 2018 57, 173 pts; Matthews 2018 66, 137 pts; Kongpolprom 2018 509, 51 pts; Greer 2013 (a) 1546, 59 pts] absent corneal reflex at 72h-day 7 predicted poor neurologic outcome from hospital discharge to 12 months with specificity ranging from 98.8% to 100% and sensitivity ranging from 23.1% to 64.1% (very-low certainty of evidence).

Myoclonus

Myoclonus was investigated in eight studies [Sadaka 2015 292; Fatuzzo 2018 29; Rossetti 2017 e674; Kongpolprom 2018 509; Sivaraju 2015 1264; Dhakar 2018 114; Lybeck 2017 146; Reynolds 2018 249].

In eight studies [Sadaka 2015 292, 58 pts; Fatuzzo 2018 29, 493 pts; Rossetti 2017 e674, 367 pts; Kongpolprom 2018 509, 51 pts; Sivaraju 2015 1264, 100 pts; Dhakar 2018 114, 59 pts; Lybeck 2017 146, 933 pts; Reynolds 2018 249, 583] presence of myoclonus within 96h predicted poor neurological outcome from hospital discharge to 6 months with specificity ranging from 77.8% to 97.8% and sensitivity ranging from 18.2% to 39.6% (very-low certainty of evidence).

Definitions of myoclonus were provided in only three of these eight studies [Sadaka 2015 292; Dhakar 2018 114; Lybeck 2017 146]. These definitions differed among studies.

Status myoclonus

Status myoclonus was investigated in two studies [Ruknuddeen 2015 304, 121 pts; Zhou 2019 343, 226 pts]. In these two studies, presence of status myoclonus within 72h predicted poor neurological outcome from hospital discharge to 6 months with specificity ranging from 97.0% to 100% and sensitivity ranging from 30.6% to 49.1% (very-low certainty of evidence).

Status myoclonus was not defined in Zhou, 2019. In Ruknuddeen 2015 304, status myoclonus was defined as “spontaneous or sound-sensitive, repetitive, irregular brief jerks in both face and limb present most of the day within 24 h post-CA”. This definition was derived from Wijdicks 1994 239.

Treatment recommendations

  • We suggest using pupillary light reflex at 72h or later after ROSC for predicting neurological outcome of adults who are comatose after cardiac arrest (weak recommendation, very-low-certainty evidence).
  • We suggest using quantitative pupillometry at 72h or later after ROSC for predicting neurological outcome of adults who are comatose after cardiac arrest (weak recommendation, low-certainty evidence).
  • We suggest using bilateral absence of corneal reflex at 72h or later after ROSC for predicting poor neurological outcome in adults who are comatose after cardiac arrest (weak recommendation, very low-certainty evidence).
  • We suggest using presence of myoclonus or status myoclonus within 96h after ROSC, in combination with other tests, for predicting poor neurological outcome in adults who are comatose after cardiac arrest (weak recommendation, very low-certainty evidence). We also suggest recording EEG in presence of myoclonic jerks in order to detect an associated epileptiform activity.

Justification and Evidence to Decision Framework Highlights

As for the 2015 CoSTR on this topic, the Task Force opinion is that a multimodal approach should be used in all cases with all supplementary tests considered in the context of the clinical examination.

For standard pupillary light reflex, limited evidence suggests that the highest specificity for prediction of poor neurological outcome is achieved at 72h or later after cardiac arrest. This may be partly due to confounding from the effect of sedatives used for TTM or to facilitate ventilation. Only some of the included studies specifically excluded the presence of residual sedation at the time PLR was assessed. Lack of blinding is a major limitation of PLR, even if WLST based on PLR only has not been documented in any of the studies included in our review. Despite its limitations, given the ease of assessment and the minimal equipment required, the balance between the costs and benefits favours benefits.

Limited evidence suggests that pupillometry using NPi achieves 100% specificity for prediction of poor neurological outcome as early as 24h after cardiac arrest. The choice of 72h for this recommendation has been made based on parallel evidence regarding s-PLR, on the lower likelihood of persisting effects from sedation at that time point, and on the fact that specificity of a qPLR seems to increase from 24h to 72h. However, the number of available studies is still low and no consistent qPLR or NPi threshold for 100% poor outcome has been identified. Although in some of the studies the treating team was blinded to results of pupillometry, a correlation with standard PLR, which cannot be blinded, is likely. WLST based on results of pupillometry has not been documented in any of the studies included in our review. Because of its high specificity and the standardized assessment parameters, the balance between the costs and benefits favours benefits

Low-certainty evidence suggests that prediction of poor neurological outcome using CR can be made with high specificity at 72h or later after cardiac arrest. This predictor is prone to confounding due to the effects of sedatives or muscle relaxants used for TTM or to facilitate ventilation. Only part of the included studies specifically excluded the presence of residual sedation or paralysis at the time CR was assessed. Lack of blinding is a major limitation of CR, however WLST based on CR only has not been documented in any of the studies included in our review and appears to be unlikely. Despite its limitations, given the easiness of assessment and the minimal costs and required equipment, the balance between the costs and benefits favours benefits. Combining CR with other predictors is reasonable.

Although the definitions of both myoclonus and status myoclonus are absent or inconsistent in most studies, the presence of myoclonus is associated with poor outcome in patients who are comatose after resuscitation from cardiac arrest and it may be useful within the context of a multimodal prognostic assessment. Myoclonus and status myoclonus are inconsistently associated with epileptiform activity on the EEG.

Knowledge Gaps

Absence of residual effects from sedatives needs to be specifically assessed in studies evaluating the accuracy of predictors based on clinical examination after cardiac arrest.

The interrater agreement for the assessment of standard pupillary light reflex, corneal reflex, and myoclonus/status myoclonus in patients resuscitated from cardiac arrest deserves investigation.

The number of studies documenting pupillometry for predicting poor outcome after cardiac arrest is still low. A consistent threshold for 100% specificity has not been identified for either qPLR or NPi.

Achieving a uniform and consensus-based definition of both myoclonus and status myoclonus is necessary. The role of EEG as an additional tool to investigate the nature and the prognostic significance of myoclonus deserves investigation.

The most reliable combination and timing for each assessment remains to be determined.

Attachments

  1. Evidence-to-Decision Table: PLR ETD
  2. Evidence-to-Decision Table: Pupillometry ETD
  3. Evidence-to-Decision Table: Corneal ETD
  4. Evidence-to-Decision Table: Myoclonus Status Myoclonus ETD

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