American Journal of Emergency Medicine xxx (2016) xxxxxx

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American Journal of Emergency Medicine

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Original Contribution

Serum potassium concentration predicts brain hypoxia on computed

tomography after avalanche-induced cardiac arrest
Julien G. Cohen, MD a, Yvonnick Bou, MD b, Bastien Boussat, MD c,d, Emilie Reymond, MD a,
Sylvie Grand, MD a,e,f, Marc Blancher, MD g, Gilbert R. Ferretti, MD, PhD a,f, Pierre Bouzat, MD, PhD b,e,f,
a
Ple Imagerie, Centre Hospitalier Universitaire de Grenoble, CS 10217, F-38043 Grenoble, France
b
Ple Anesthsie Ranimation, Centre Hospitalier Universitaire de Grenoble, CS 10217, F-38043 Grenoble, France
c
Ple Sant Publique, Centre Hospitalier Universitaire de Grenoble, CS 10217, F-38043, Grenoble, France
d
Laboratoire Techniques de l'Ingnierie Mdicale et de la Complexit, CNRS UMR5525, F-38043 Grenoble, France
e
Grenoble Institut des Neurosciences, INSERM U836, F-38043 Grenoble, France
f
Grenoble Alpes Universit, F-38043 Grenoble, France
g
Ple Urgence-Mdecine Aigu, Centre Hospitalier Universitaire de Grenoble, CS 10217, F-38043 Grenoble, France

a r t i c l e i n f o a b s t r a c t

Article history: Background: Brain anoxia after complete avalanche burial and cardiac arrest (CA) may occur despite adequate on-
Received 27 November 2015 site triage.
Received in revised form 29 January 2016 Purpose: To investigate clinical and biological parameters associated with brain hypoxia in a cohort of avalanche
Accepted 31 January 2016 victims with whole body computed tomographic (CT) scan.
Available online xxxx
Methods: Retrospective study of patients with CA and whole body CT scan following complete avalanche burial
admitted in a level-I trauma center.
Main ndings: Out of 19 buried patients with whole body CT scan, eight patients had refractory CA and 11 patients
had pre-hospital return of spontaneous circulation. Six patients survived at hospital discharge and only two had
good neurologic outcome. Twelve patients had signs of brain hypoxia on initial CT scan, dened as brain edema,
loss of gray/white matter differentiation and/or hypodensity of basal ganglia. No clinical pre-hospital parameter
was associated with brain anoxia. Serum potassium concentration at admission was higher in patients with brain
anoxia as compared to patients with normal CT scan: 5.5 (4.17.2) mmol/L versus 3.3 (3.04.2) mmol/L,
respectively (P b .01). A threshold of 4.35 mmol/L serum potassium had 100% specicity to predict brain anoxia
on brain CT scan.
Conclusions: Serum potassium concentration had good predictive value for brain anoxia after complete avalanche
burial. This nding further supports the use of serum potassium concentration for extracorporeal life support
insertion at hospital admission in this context.
2016 Elsevier Inc. All rights reserved.

1. Introduction
Mortality rate after complete avalanche burial is around 52% [1] due
to asphyxia, severe trauma and/or deep hypothermia [2,3]. Asphyxia
and severe trauma are the leading cause of cardiac arrest (CA) in this
context and are associated with poor neurologic outcome [25].
Conversely, CA due to accidental hypothermia is rare but may confer
ideal condition for successful neurological recovery despite prolonged
avalanche burial [6,7]. On-scene triage of avalanche victims with CA
aims at identifying patients with isolated accidental hypothermia to
be resuscitated until rewarming. Triage algorithms are based upon
Corresponding author at: Ple d'Anesthsie-Ranimation, Hpital Albert Michallon,
BP 217, F-38043, Grenoble, France. Tel.: +33 4 76 76 92 88; fax: +33 4 76 76 51 83.
E-mail address: PBouzat@chu-grenoble.fr (P. Bouzat).
duration of burial, airway conditions, body core temperature, initial car-
diac activity and reported signs of life at extrication [8]. After on-scene
triage, updated recommendations for extracorporeal life support
(ECLS) relies on body core temperature lower than 30 C, duration of
burial longer than 60 minutes, no severe trauma and serum potassium
concentration lower than 8 mmol/L at hospital admission [9]. Despite
adequate adherence to algorithms, patients with brain anoxia are still
admitted to the Emergency Department (ED), which challenges the
usefulness of the applied criteria.
Only limited data are available regarding CT scan ndings after com-
plete avalanche burial and mainly focus on traumatic injuries [10,11].
However, signs of brain anoxia on cerebral CT scan would be relevant
to further explore the association between clinical/biological parame-
ters and neurological prognosis. Moreover, snow aspiration signs on
thoracic CT scan maybe also helpful to test the relevancy of airway pat-
tern assessment in the eld. As whole body imaging was performed in

http://dx.doi.org/10.1016/j.ajem.2016.01.037
0735-6757/ 2016 Elsevier Inc. All rights reserved.

Please cite this article as: Cohen JG, et al, Serum potassium concentration predicts brain hypoxia on computed tomography after avalanche-
induced cardiac arrest, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.037
2 J.G. Cohen et al. / American Journal of Emergency Medicine xxx (2016) xxxxxx
our center to assess associated injuries and potential brain anoxia in
these patients, we decided to test whether CT signs of brain hypoxia
were associated with clinical and biological parameters used for triage
of avalanche victims with CA [12,13].
2. Methods
We retrospectively studied consecutive avalanche patients admitted
in one level-I trauma center (Grenoble University Hospital, Northern
French Alps, France) from 2002 to 2014. Patients with the following
criteria were nally included: (1) complete avalanche burial, dened
as a burial concerning at least head and chest (2) on-scene cardiac
arrest, and (3) whole-body CT scan including cerebral, cervical, thoracic,
abdominal and pelvic regions. Exclusion criteria were: (1) partial burial
(2) no CT scan, and (3) post-mortem CT scan. All these patients were
part of a larger cohort used for survival assessment after avalanche
induced cardiac arrest [14]. The Regional Institutional Ethics Committee
approved the study design (Comit d'Ethique des Centers d'Investigation
Clinique de l'inter-rgion Rhne-Alpes-Auvergne, IRB number 5891,
approval on September 1, 2014).
Pre-hospital triage was done on-site by emergency physicians using
recommendations for avalanche victims' management edited before
2014 [1,3]. Briey, following CA, patients were transported to the ED if
(1) return of spontaneous circulation (ROSC) was obtained in the eld
or (2) refractory cardiac arrest by isolated accidental hypothermia was
suspected: duration of burial longer than 35 minutes and body core
temperature lower than 32 C with any signs of life reported by wit-
nesses prior to CA, cardiac activity at extrication including ventricular -
brillation, or asystole with patent airway. At hospital admission, ECLS
was inserted in patients with serum potassium concentration lower
than 12 mmol/L associated with body core temperature (measured by
esophageal probe) lower than 32 C and no obvious signs of trauma.
Clinical and biological data were extracted from the registry of the
Trauma System of the Northern French Alps and completed using pa-
tients' les if necessary. Pre-hospital data included duration of burial,
duration of no ow and low ow, body core temperature measured by
esophageal probe, initial cardiac rhythm, signs of life preceding CA, air-
way patency (air pocket, airway obstruction) and signs of severe trau-
ma. Biological data were collected upon hospital admission on a
central line: arterial blood gases, serum potassium concentration,
serum lactate concentration, coagulation parameters (activated partial
thromboplastin ratio, prothrombin ratio, brinogen, platelets count)
and hemoglobin level. Injury Severity Score was also recorded. Survival
was reported at hospital discharge and neurologic outcome of survivors
was assessed using cerebral performance category (CPC) at 3 months.
Whole-body CT scans were done under the supervision of
intensivists. The aim of whole-body imaging was to assess associated in-
juries and potential brain anoxia. CT scans were conducted using Sie-
mens Sensation 16 (Siemens, Erlangen, Germany) or Philips Brilliance
40 and 64 (Philips Medical Systems, Eindhoven, The Netherlands).
Whole body CT protocol consisted of the following acquisitions: (1) a
non-enhanced encephalic CT scan, (2) a non-enhanced CT scan of the
neck, from the base of the skull to the level of the second thoracic verte-
bra, (3) a contrast-enhanced CT scan of the thorax, abdomen and pelvic
regions from the level of the sixth cervical vertebra to the lesser tro-
chanter, (4) a contrast-enhanced scan of the abdomen from the dia-
phragmatic dome to the lesser trochanter. Arms were placed above
the head after the CT scan of the head and neck. Optionally, mainly
when a severe cervical traumatism was suspected, a CT angiography
of arterial supra-aortic vessels was added. Regarding contrast-medium
injection, a 120-mL bolus of iso-osmolar, non-ionic iodinated contrast
material [350 mg iodine/ml, Iohexol (Omnipaque 350; GE Healthcare)]
followed by a saline ush of 40 mL was injected into an antecubital vein
at a ow rate of 4 mL/s. The data acquisition was initiated 6 seconds
after 100 Hounseld Units (HU) attenuation in the descending thoracic
aorta. After a further delay of 45 s, the abdominal portal-venous
Please cite this article as: Cohen JG, et al, Serum potassium concentration predicts brain hypoxia on computed tomography after avalanche-
induced cardiac arrest, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.037
enhanced phase was acquired. For supra-aortic vessel acquisition, an
additional injection of 120 mL of the same contrast medium was done,
and acquisition was triggered at 75 HU attenuation in ascending aorta.
Three trained radiologists reviewed all whole body CT scans. In-
volved physicians included one neuroradiologist, one chest radiologist,
and one general radiologist. For each patient, radiologists interpreted
traumatic and non-traumatic lesions according to the methodology de-
scribed in Supplemental le no. 1. Brain hypoxia was dened as brain
edema, loss of white/gray matter differentiation, and/or hypodensity
of basal ganglia. In order to further study radiologic pattern of snow as-
piration, and since there is no gold standard for this condition, we pro-
posed dening snow aspiration using the following methodology. First
we identied all patients with lung parenchyma abnormalities. We ex-
cluded those with isolated gravity-related lung opacities. We checked
CT scans of remaining patients for signs of thoracic traumatic injuries,
which were dened as fractures of ribs, sternum, clavicles, thoracic ver-
tebrae and the presence of a pneumo- or hemothorax. Traumatic inju-
ries associated with resuscitation were dened as isolated fractures of
anterolateral ribs and/or sternum in patients with known cardiac resus-
citation [15]. Lung opacities with no associated signs of thoracic trauma
(not including traumatic injuries due to resuscitation) were considered
as snow aspiration. Traumatic injuries in the whole body were also an-
alyzed using the CT features described in Supplemental le no. 1.
Data were expressed as median and 25th to 75th percentiles. Cate-
gorical variables were compared using the Fisher exact test for two-
by-two tables and the FreemanHalton extension for 2 3 tables. Con-
tinuous variables were compared using Wilcoxon rank sum test. Multi-
variate analysis was not conducted given the low number of patients.
The properties of serum potassium concentration on admission for
brain hypoxia prediction were also tested using receiver operating
curve (ROC) analysis. Maximization of the Youden index [16] was
used to determine the best threshold. Density function was employed
to generate a smooth kernel density ROC curve [17]. 95% condence in-
tervals of the areas under the curve were yielded using Delong method
for the empirical curve [18] and stratied bootstrap from 1000 repli-
cates for the smooth curve [19]. Statistical analysis was done with
Stata 12 software. P b .05 was declared statically signicant.
3. Results
Thirty-nine patients with whole-body imaging were admitted to the
ED following avalanche burial within the study period. Only 19 patients
met the inclusion criteria for the nal analysis (see ow chart in Fig. 1).
Pre-hospital characteristics of the study population are shown in
Table 1. The median duration time of cardiopulmonary resuscitation
was 70 minutes (15420 minutes). Eight patients were transferred to
the ED with refractory CA and 11 patients had pre-hospital ROSC. All pa-
tients with refractory CA received ECLS at hospital admission. Eight pa-
tients had traumatic injuries but only 2 patients presented Injury
Severity Score higher than 15. Detail of injuries is described in Supple-
mental le no. 2. Biological parameters are reported in Table 2. Six pa-
tients (32%) survived at hospital discharge. CPC score was 1 (no
disability) for 2 patients, 3 (severe disability) for 1 patient and 4 (vege-
tative state) for 3 patients. The 2 patients with good neurologic outcome
had initial pulseless electrical activity at extrication before refractory CA
and ECLS implantation. All patients with initial asystole and refractory
CA did not survive (n = 6 patients). In the non-survivor patients
(n = 13 patients), causes of death were brain death for 11 patients
(85%) and multiple organ failure for 2 patients (15%).
Out of 19 patients, 12 (63%) patients had signs of brain hypoxia on
cerebral imaging. One patient had isolated brain edema whereas 11 pa-
tients had diffuse edema associated with loss of gray/white matter dif-
ferentiation. Univariate analysis between patients with brain hypoxia
(n = 12 patients) and patients with normal cerebral CT scan (n = 7 pa-
tients) is presented in Table 3. No clinical prehospital parameter was
 J.G. Cohen et al. / American Journal of Emergency Medicine xxx (2016) xxxxxx 3

the diagnosis of brain hypoxia. Although jagged, empirical ROC curve

was consistent with the smooth kernel density ROC curve and its
bootstrapped 95% condence interval, ie, 0.88 (95% CI 0.78-0.93).

4. Discussion

In this series of avalanche victims with CA and whole body CT scan,

Fig. 1. Flow chart of the study population.
associated with brain hypoxia on CT scan. For instance, only 1 patient
out of 12 patients with brain hypoxia presented with an airway obstruc-
tion in the eld. Snow aspiration assessed by lung imaging was also not
different between the 2 groups. Regarding biological data, serum
potassium concentration was higher in patients with brain hypoxia as
compared to normal CT scan patients: 5.5 (4.1-7.2) mmol/L vs 3.3
(3.0-4.2) mmol/L, respectively (P b .01). Patients with brain hypoxia
had also more coagulation disorders as compared to the normal CT
scan patients.
ROC curve analysis to predict brain hypoxia with serum potassium
concentration at hospital admission is represented in Fig. 2. Area
under the empirical ROC curve was 0.91 (95% CI 0.78-1.00). The thresh-
old of 4.35 mmol/L had a sensitivity of 67% and specicity of 100% for
Table 1
Pre-hospital characteristics of the 19 studied patients
clinical parameters in the eld were not associated with brain hypoxia
on cerebral CT scan. At hospital admission, serum potassium concentra-
tion was found to be a good predictor of brain hypoxia. The threshold of
4.35 mmol/L reached 100% specicity. These ndings highlighted the
role of serum potassium concentration on admission to help clinical de-
cision for ECLS insertion at hospital.
Overall mortality in our study was 68% and was mainly related to
global cerebral ischemic injuries occurring in 12 out of 19 patients.
This rate was higher than previously reported mortality. For instance,
in a cohort of 1886 Swiss avalanche victims, overall mortality was
23%. However, this proportion rose to 52.4% in patients with complete
burial [1]. In our cohort, elevated mortality maybe related to specic se-
lection of patients with CA and complete avalanche burial. This nding
was in line with recent publication focusing on CA after avalanche burial
[20]. Brain hypoxia was the leading cause of mortality in our cohort. Loss
of gray/white matter differentiation was the prominent cerebral imag-
ing pattern, also known as the loss of boundary sign. This specic ce-
rebral nding has been described after CA and was found to be strongly
associated with time to ROSC. Indeed, the incidence of this pattern was
23% when ROSC occurred within 20 minutes and increased up to 83%
after 20 minutes [21]. Interestingly, signs of cerebral edema on CT
scan were frequently found after CA related to asphyxia [22]. In a cohort
of 51 patients with out-of-hospital CA, loss of gray/white differentiation
was also associated with poor neurologic outcome [23]. Taken together,
these ndings conrmed the high proportion of asphyxia in our series
resulting in poor outcome.
Clinical pre-hospital parameters used for on-scene triage were not
associated with brain hypoxia. This nding underlined the poor predic-
tive value of each clinical sign to rule out asphyxia after complete ava-
lanche burial and CA. This concept was further supported by
international guidelines, which recommended transferring patients to
hospital when deep hypothermia was strongly suspected in the eld re-
gardless of pre-hospital clinical parameters [3]. No association was also
found between snow aspiration on lung CT scan and brain hypoxia. In-
deed, asphyxia may be more related to rebreathing of expired CO2 due
to limited or no air pocket rather than acute airway obstruction by
snow and/or ice mask. We also believe that snow aspiration maybe
underestimated on admission CT since snow water is hypotonic and
gets quickly absorbed through pulmonary and systemic circulation,
similarly to fresh water drowning [24].

Variables Values Table 2

Age (years) 36 (2341) Biological data of the 19 studied patients on hospital admission
Male gender (number) 16
Variables Values
Prehospital body core temperature (C) 27.9 (26.030.2)
Burial time (min) 30 (2045) Serum potassium (mmol/L) 4.2 (3.95.7)
Maximum duration of no ow (min) 25 (2040) Serum sodium (mmol/L) 138 (137143)
Duration of low ow (min) 20 (10110) Arterial pH 7 (6.67.2)
Prehospital cardiac rhythm (number): PaCO2 (mmHg) 40 (3260)
Asystole 15 PaO2 (mmHg) 361 (150558)
Ventricular brillation 1 Serum bicarbonate (mmol/L) 10 (514)
Pulseless electrical activity 3 Serum lactate (mmol/L) 11.8 (8.114.2)
Return of spontaneous circulation (number) 11 Hemoglobin (g/L) 146 (128160)
Transport under CPR (number) 8 Platelets (G/L) 154 (121204)
Vital signs preceding CA (number) 3 Activated Partial Thromboplastin ratio 1.82 (1.314.1)
Prehospital trauma signs (number) 4 Prothrombin ratio (%) 52 (3061)
Prehospital airway obstruction (number) 1 Serum brinogen (g/L) 1.6 (0.81.9)
Air pocket (number) 3 Serum creatinine (mol/L) 140 (118184)
Serum glucose (mmol/L) 15.1 (11.318.6)
Values are expressed as median and 25-75th percentiles. CPR, cardiopulmonary re-
suscitation; CA, cardiac arrest. Values are expressed as median and 25-75th percentiles.

Please cite this article as: Cohen JG, et al, Serum potassium concentration predicts brain hypoxia on computed tomography after avalanche-
induced cardiac arrest, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.037
4 J.G. Cohen et al. / American Journal of Emergency Medicine xxx (2016) xxxxxx

Table 3
Univariate analysis between patients with brain hypoxia on cerebral CT scan (n = 12 patients) and patients with normal cerebral CT scan (n = 7 patients).

Variable No brain hypoxia (n = 7 patients) Brain hypoxia (n = 12 patients) p-value

Burial time (min) 35 (22360) 27.5 (2042.5) 0.42

Core temperature (C) 26.5 (23.330.1) 28.0 (26.832.0) 0.24
Signs of life, n 2 1 0.52
Airway obstruction, n 0 1 1
Air pocket, n 2 1 0.52
Prehospital cardiac rhythm 0.70
Asystole, n 5 10
Ventricular brillation, n 0 1
Pulseless electrical activity, n 2 1
Prehospital ROSC, n 5 6 0.63
ECLS, n 2 6 0.63
Serum potassium (mmol/L) 3.3 (3.04.2) 5.5 (4.17.2) b0.01
pH 7.2 (6.87.2) 6.9 (6.57.1) 0.19
PaO2 (mmHg) 432 (334664) 275 (64486) 0.18
PaCO2 (mmHg) 36 (3550) 53 (31133) 0.31
Bicarbonate (mmol/L) 15 (518) 10 (713) 0.15
Lactate (mmol/L) 8.1 (6.421.3) 12.6 (9.814.2) 0.18
Hemoglobin (g/dl) 146 (124158) 148 (133160) 0.61
Platelet (G/L) 166 (132214) 143.5 (120.0184.5) 0.29
APT ratio 1.3 (0.81.6) 2.8 (1.75.2) 0.03
PR (%) 58 (5587) 41 (2856) 0.01
Fibrinogen (g/L) 1.7 (1.62.7) 1.3 (0.71.8) 0.05
CPC 1-2, n 2 0 0.12
Death, n 1 12 b0.001
Snow aspiration imaging, n 5 9 1

Values are expressed as median and 25-75th percentiles. ROSC, return of spontaneous circulation; ECLS, extracorporeal life support; APT, Activated Partial Thromboplastin ratio; PR, pro-
thrombin ratio; CPC, cerebral performance category.

Regarding biological parameters, serum potassium concentration on
hospital admission was associated with brain hypoxic damage in our co-
hort. This biological parameter also showed good AUC to predict brain
hypoxia. Serum potassium concentration has been extensively studied
in avalanche victims for in-hospital triage in retrospective case
control studies [2527] and case reports [6,2830]. In a retrospective
study of 32 hypothermic avalanche victims, serum potassium at
Fig. 2. Empirical receiving operator curve (ROC, black line) and smooth kernel density ROC
curve (dash line) of serum potassium concentration to predict brain hypoxia. Serum po-
tassium concentration was measured at hospital admission on a central line. Brain hypoxia
was dened by experienced neuroradiologist as isolated brain edema, loss of white/gray
matter differentiation and/or hypodensity of basal ganglia.
hospital admission was lower in survivors compared to non survivors
(4.25 4.9 mmol/L vs 9.95 4.9 mmol/L, respectively). The highest ad-
mission serum potassium associated with survival after avalanche-
induced cardiac arrest was 6.4 mmol/L but no information was given re-
garding neurologic outcome [25]. To our knowledge, our study was the
rst to demonstrate an association between serum potassium concen-
tration and cerebral CT signs of hypoxia. Guidelines for avalanche vic-
tims' management now recommend stopping resuscitation in patients
with refractory CA when serum potassium concentration is higher
than 8 mmol/L [9]. ROC analysis in our study revealed that the threshold
for irreversible brain damage was lower. Indeed, serum potassium con-
centration of 4.35 mmol/L had 100% specicity to diagnose brain ische-
mia on CT scan. This result supported the lowering of serum potassium
cut-off for in-hospital triage. Nevertheless, the small sample size of our
study did not allow us to draw rm conclusion regarding this threshold.
We also found coagulation disorders to be associated with brain hypox-
ia. Interestingly, initial coagulopathy was associated with poor neuro-
logic outcome in a cohort of 252 patients with out-of-hospital CA [31].
However, coagulation assessment could be challenging at the bedside
and the role of coagulopathy for in-hospital triage deserves further
exploration.
We acknowledge several limits to our study. This work was a small
sample size retrospective study and the present case series illustrated
rare conditions since only hemodynamically stable avalanche victims
were transported to CT scan. The limited number of patients in each cat-
egory should temper our conclusions down. Accordingly, the serum po-
tassium threshold should not be generalized for every avalanche
patient. However, performing a large study is challenging due to low in-
cidence of complete avalanche burial and cardiac arrest. Data regarding
whole body imaging after avalanche burial are scarce and this study
adds further insights about factors associated with brain hypoxia in
this context. The implementation of an international registry will over-
come this limitation in future studies.
In conclusion, serum potassium concentration had good predictive
value for brain hypoxia prediction after complete avalanche burial and
cardiac arrest. This biological parameter is a key element for in-
hospital triage to insert ECLS after refractory CA. Pre-hospital clinical pa-
rameters were not associated with brain hypoxia in our cohort, which

Please cite this article as: Cohen JG, et al, Serum potassium concentration predicts brain hypoxia on computed tomography after avalanche-
induced cardiac arrest, Am J Emerg Med (2016), http://dx.doi.org/10.1016/j.ajem.2016.01.037
 J.G. Cohen et al. / American Journal of Emergency Medicine xxx (2016) xxxxxx
challenged the relevancy of such parameters to predict cerebral
ischemic damages.
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.ajem.2016.01.037.
Conict of interest
None.
Acknowledgments
None.
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