www.elsevier.com/locate/jelectrocard

Journal of Electrocar

Electrocardiographic changes by accidental hypothermia in an

urban and a tropical region

Dilma de Souza, MD,a Andres Ricardo Perez Riera, MD,b Maria Teresa Bombig, MD,a

Yona Afonso Francisco, MD,a Luigi Brollo, MD,a Braulio Luna Filho, MD, PhD,a

Sergio Dubner, MD,c Edgardo Schapachnik, MD,d Rui Povoa, MDa,4aEscola Paulista de Medicina, UNIFESP, Sao Paulo CEP, Brazil

bSector of Electro-Vectocardiography of the Discipline of Cardiology, School of Medicine, ABC Foundation, Santo Andre, Sao Paulo CEP, BrazilcArrhythmias and Electrophysiology Service, Clinical and Maternidad Suizo, Argentina, Buenos Aires, Argentina

dDepartment of Chagas Disease, Dr Cosme Argerich Hospital, Buenos Aires, Argentina

Received 5 May 2006; accepted 28 August 2006

Abstract Background: Hypothermia is defined as a condition in which core temperature (rectal, esophageal,

0022-0736/$ – see fro

doi:10.1016/j.jelectroc

4 Corresponding

E-mail address: rm

or tympanic) reaches values below 358C. This may be accidental, metabolic, or therapeutic. The

accidental form is frequent in cold-climate countries and rare in those with tropical or subtropical

climate. The aim of this study was to evaluate electrocardiographic changes of patients with

accidental hypothermia.

Methods: In 59 patients with hypothermia, the following electrocardiogram parameters were

analyzed: rhythm and heart rate (HR), P-wave characteristics, PR-interval duration, QRS-complex

duration, presence of J wave and its location characteristics, polarity, voltage, aspect and its

correlation with the degree of hypothermia, changes in T wave regarding its polarity and

characteristics, duration of the QT interval corrected for HR using both Bazett and Friderica

formulas, and possible presence of both supraventricular and ventricular arrhythmias were

independently and blindly analyzed in the tracings by experienced cardiologists.

Results: In 6 patients, electrocardiogram was normal. Sinus bradycardia was observed in 52.5% of

the patients. J wave was present in 51 patients, and its voltage correlated inversely and was

statistically significantly with the core temperature. Changes in T wave were observed in 47.4% of

the cases. QT interval, adjusted for HR, was prolonged in 72.8% of the cases. Idioventricular rhythm

was found in 6 cases, total atrioventricular block in 3 cases, and junctional rhythm and atrial

fibrillation in 2 patients.

Conclusions: Electrocardiogram changes in accidental hypothermia are frequent and characteristic

for this entity improving diagnosis in usually unconscious patients, and in many cases, it may be the

diagnostic clue in patients with conscience deficit in emergency units, even in patients from a

tropical climate where the population at risk may be exposed to temperatures below 208C.

D 2007 Elsevier Inc. All rights reserved.

Keywords: Accidental hypothermia; J waves; Electrocardiogram

Introduction

Presently, hypothermia is defined as a clinical condition

in which internal or core temperature (rectal, esophageal, or

tympanic) is less than 358C.1

The hypothermic state is characterized by fall in basal

metabolism, decrease in oxygen consumption, and greater

carbon dioxide production.2

nt matter D 2007 Elsevier Inc. All rights reserved.

ard.2006.08.094

author. Tel.: +55 11 5549 9395.

spovoa@cardiol.br

Cardiovascular effects include gradual heart rate (HR)

and cardiac output decrease. Systemic blood pressure

progressively falls with the fall in body temperature.

Clinically important arterial hypotension occurs when core

temperature reaches values below 258C.3

Body temperature reduction induces characteristic elec-

trophysiologic changes: the HR is markedly reduced by a

reduction in the diastolic depolarization rate of the sinoatrial

node P cells, and conduction becomes slow and is expressed

as prolongation of the PR interval, the QRS complex, and

the QT interval. There is also a decrease in the level of

diology 40 (2007) 47–52

D. de Souza et al. / Journal of Electrocardiology 40 (2007) 47–5248

resting potential associated with marked prolongation of the

action potential (AP) and refractory period attributed to slow

repolarization. These electrophysiologic phenomena explain

QTc-interval prolongation.

Atrial fibrillation is found in a large percentage of cases

(50%-60%) and on average emerges when core temperature

reaches 298C and is associated with a higher mortality.4

There are studies showing that older age range is a

significant conditioner of atrial fibrillation emergence in

hypothermia.5

Ventricular fibrillation may be observed when core

temperature reaches values between 288C and 308C. If it

occurs at higher temperatures, association with preexisting

myocardial disease or increase in transmyocardial temper-

ature should be suspected.6

Accidental hypothermia has a much higher incidence

in cold-climate countries. The city of Sao Paulo, in the

southeastern region of Brazil, has a tropical climate with mild

temperatures presenting annual averages of 208C to 258C.The objective of this study was to analyze changes in

electrocardiograms (ECGs) of 59 patients hospitalized in the

intensive care unit of a public hospital of the city of Sao

Paulo with diagnosis of accidental hypothermia.

Fig. 1. Typical ECG of patient with hypothermia showing extreme sinus bradyc

complex and the ST segment, especially visible in inferior and V5 through V6 le

Methods

This is a retrospective and observational study. The

sample consisted of 59 patients (38 men), with a mean age

of 37.2 F 16.3 years (21-79 years) admitted into the

intensive care unit in a municipal emergency public hospital

in the period between 1985 and 2003.

On admission, a 12-lead ECG was performed and the

core temperature taken with a Hewlett-Packard rectal

thermometer left for a minimum of 4 minutes. Sodium,

potassium, chloride determinations, and arterial gasometry

were performed in all patients. Hypothermia was considered

to be present when the rectal temperature measured during

4 minutes or longer was equal to or below 358C. Mild

hypothermia was defined as a rectal temperature between

338C and 34.98C; moderate hypothermia, between 288C and

32.98C; and severe hypothermia, when below 288C.Twelve-lead ECGs were recorded soon after admission in

the 59 cases and repeated, for each 38C to 48C rise in

temperature, in 11 cases of the total.

Electrocardiograms were analyzed by experienced car-

diologists who did not know the clinical and laboratory

variables of the patients.

ardia at 30 beats/min, and positive deflection (J wave) between the QRS

ads.

Fig. 2. There was an inverse and significant correlation between J-wave voltage (millimeter) and core temperature.

D. de Souza et al. / Journal of Electrocardiology 40 (2007) 47–52 49

The following parameters were analyzed and measured

using a magnifying glass: cardiac rhythm and HR, P-wave

characteristics, PR-interval duration, QRS-complex dura-

tion, typical J-wave presence, T-wave characteristics, QT-

interval duration adjusted for HR (QTc) using Bazett and

Friderica formulas, and eventual presence of supraventric-

ular and/or ventricular arrhythmias.

J-wave amplitude was calculated by measuring its

voltage in the lead where it was more prominent. This

value was correlated with the other variables (core

temperature, pH, and serum electrolytes). Spearman corre-

lation test, with a level of P b .01, was used for the

statistical analysis to study the relationship between core

temperature and J-wave magnitude.

Results

In the 59 patients with accidental hypothermia, the

etiologic cause was prolonged environmental exposure to

cold associated with alcoholism, barbiturate intoxication, or

epilepsy, and in most cases, people living in the streets were

involved and it occurred always in the winter months.

Electrocardiograms were abnormal in 53 patients. In

6 patients, ECG was normal and this group of patients

presented with mild hypothermia.

Of the 59 patients, 12 presented mild, 37 moderate, and

10 severe hypothermia. Sinus rhythm was present in

44 cases (74.5%), being associated with sinus bradycardia

in 31 (52.5%) of them (HR V 60 beats/min).

A direct correlation between HR and core temperature

was observed (r = 0.456, P = .001). Thus, the greater the

fall in core temperature, the more intense the bradycardia.

The extra positive deflection between the QRS complex

and the onset of the ST segment, considered typical and

known as J wave, was more prominently observed in the

leads facing the left ventricle (V5-V6) and in the inferior

leads II, III, and aVF in 51 of the 59 patients. Fig. 1 shows

the typical ECG of hypothermia.

In agreement with the data in literature, there was an

inverse and significant correlation between J-wave voltage

(millimeter) and core temperature (degree Celsius) by

Spearman test (r = �0.594, P b .001). Fig. 2 shows the

inverted relationship between central body temperature and

J-wave voltage.

Regarding J wave, we studied location, polarity, voltage,

aspect, and degree of hypothermia. The J wave is located at

the point of QRS complex ending (late d wave) occupying

the initial part of the ST segment corresponding to phases 1

and 2 of AP.7 The J wave is always positive and prominent in

the leads facing the left ventricle—V5 and V6—and possibly

mainly in hearts in vertical position in inferior wall leads,8

differently from the J wave found in Brugada syndrome

located in the right precordial leads V1 to V2 or V3.

The J wave has a slow and lasting inscription, and a

higher voltage in the left V5 and V6 leads, and is inversely

proportional to the severity of hypothermia; that is, the

lower the core temperature, the higher the voltage in J wave.

In certain cases, J wave acquires high voltage associated

with superior convexity mimicking evolving myocardial

infarction, which reverts with normalization of core

temperature.9 Eventually, the J wave may appear simulating

to be a small secondary R wave (RV).The J wave is observed during the last phase of

hypothermia, when the core temperature is below 258C(exhaustion phase).

In 2 patients, it was not possible to identify J wave in

spite of hypothermia being severe because of concomitant

idioventricular rhythm, which probably hid the wave.

Changes in ventricular repolarization, prolongation of PR

and QTc intervals for HR, and arrhythmias were observed.

Among all of the patients, QTc interval greater than

0.44 seconds was observed in 37 patients and QTc interval

greater than 0.50 seconds in 25 patients. There was

statistically significant and inverse correlation by the test of

Spearman between the QTc interval (r = �0.298, P = .02).

Table 1 shows the electrocardiographic characteristics of

59 patients with accidental hypothermia in a tropical area.

Discussion

The findings in ECG of patients with hypothermia

include sinus bradycardia, PR interval and QT/QTc interval

D. de Souza et al. / Journal of Electrocardiology 40 (2007) 47–5250

prolongation, widening of the QRS complex, supraventric-

ular and ventricular arrhythmias, and the most notable

abnormality, the appearance of an extra wave at the end of

QRS and onset of ST segment: the J wave, despite being a

Table 1

Electrocardiographic characteristics of 59 patients with accidental hypothermia in

Patient Rhythm HR

(beats/min)

Duration

of QRS (s)

QT interval

(s)

QTc

(s)

1 Sinus bradycardia 31 0.08 0.96 0.69

2 Sinus bradycardia 28 0.10 0.72 0.49

3 Total AVB 18 0.08 1.00 0.54

4 Nonclassifiable 31 0.10 0.76 0.54

5 Atrial fibrillation 82 0.08 0.64 0.78

6 Sinus bradycardia 45 0.06 0.36 0.31

7 Sinus 62 0.08 0.64 0.65

8 Sinus 78 0.08 0.48 0.54

9 Sinus bradycardia 48 0.10 0.60 0.53

10 Idioventricular 12 0.18 0.84 0.37

11 Total AVB 42 0.06 0.60 0.50

12 Idioventriculara 40 0.08 0.68 0.55

13 Atrial fibrillation 57 0.08 0.32 0.31

14 Sinus bradycardia 36 0.08 0.68 0.52

15 Idioventriculara 37 0.08 0.64 0.50

16 Sinus bradycardia 53 0.06 0.68 0.63

17 Sinus 68 0.08 0.44 0.46

18 Sinus bradycardia 37 0.08 0.52 0.40

19 Sinus bradycardia 48 0.06 0.56 0.50

20 Nonclassifiable 42 0.08 0.60 0.50

21 Sinus 52 0.04 0.60 0.55

22 Sinus bradycardia 41 0.10 0.84 0.69

23 Sinus bradycardia 50 0.08 0.64 0.58

24 Sinus bradycardia 50 0.10 0.52 0.47

25 Total AVB 57 0.04 0.52 0.50

26 Sinus 60 0.06 0.44 0.44

27 Sinus bradycardia 35 0.06 0.76 0.58

28 Sinus bradycardia 44 0.04 0.68 0.58

29 Sinus bradycardia 51 0.10 0.64 0.59

30 Sinus bradycardia 45 0.08 0.58 0.50

31 Sinus bradycardia 51 0.04 0.36 0.33

32 Sinus 62 0.06 0.40 0.40

33 Sinus bradycardia 45 0.04 0.51 0.44

34 Sinus bradycardia 45 0.08 0.41 0.35

35 Junctional 71 0.06 0.52 0.56

36 Sinus bradycardia 51 0.06 0.58 0.53

37 Sinus 45 0.08 0.34 0.29

38 Idioventriculara 31 0.10 0.54 0.38

39 Sinus bradycardia 33 0.06 0.47 0.34

40 Sinus bradycardia 48 0.08 0.58 0.51

41 Idioventriculara 27 0.10 0.59 0.39

42 Sinus 60 0.08 0.42 0.42

43 Idioventricular 20 0.14 0.84 0.48

44 Junctional 32 0.06 o.96 0.70

45 Sinus bradycardia 46 0.08 0.58 0.50

46 Sinus 50 0.06 0.48 0.43

47 Sinus bradycardia 35 0.08 0.70 0.53

48 Sinus 45 0.08 0.58 0.50

49 Sinus bradycardia 47 0.08 0.76 0.67

50 Sinus 60 0.06 0.40 0.40

51 Sinus bradycardia 41 0.06 0.68 0.56

52 Sinus bradycardia 27 0.08 0.80 0.53

53 Sinus bradycardia 36 0.08 0.72 0.55

54 Sinus 68 0.06 0.36 0.38

55 Sinus 62 0.08 0.32 0.32

56 Sinus 65 0.08 0.34 0.35

57 Sinus 72 0.10 0.34 0.37

58 Sinus 64 0.08 0.40 0.41

59 Sinus bradycardia 58 0.08 0.38 0.37

a Idioventricular with narrow QRS-complex escape rhythm. AVB, atrial vent

characteristic of hypothermia, is not an exclusive feature of

this condition. The J wave has several denominations: the

humpback or camel-hump sign,10 the humplike deflection,11

the lesion potential, and the eponym Osborn wave. The

a tropical area

interval QTc Friderica

(s)

T wave J-wave

voltage (mm)

Core temperature

(8C)

0.77 Inverted 14.5 24.5

0.55 Inverted 19.0 28.0

0.66 Flattened 5.0 30.5

0.60 Normal 5.0 28.0

0.71 Inverted 1.0 30.0

0.32 Normal 4.5 32.6

0.64 Inverted 1.5 32.1

0.59 Inverted 9.5 29.2

0.55 Flattened 3.5 29.8

0.49 Inverted Absent 22.7

0.53 Inverted 2.5 28.0

0.59 Inverted 8.5 27.0

0.31 Flattened 3.5 31.5

0.57 Flattened 2.0 33.4

0.54 Inverted 3.5 32.6

0.65 Normal 2.9 31.8

0.45 Inverted 2.0 29.8

0.44 Normal 2.5 34.0

0.51 Normal 2.5 26.8

0.53 Normal 4.5 28.9

0.57 Normal 4.5 29.2

0.73 Flattened 1.0 32.1

0.60 Normal 2.0 28.6

0.48 Flattened 2.5 30.2

0.51 Flattened 1.5 33.0

0.44 Normal 1.5 33.2

0.63 Flattened 11.0 30.0

0.61 Flattened 2.0 32.0

0.60 Normal 4.5 27.0

0.52 Inverted 7.5 29.3

0.34 Flattened 4.5 29.6

0.40 Normal 2.5 32.2

0.46 Normal 2.5 30.7

0.37 Normal 5.0 32.0

0.55 Normal 4.0 31.8

0.54 Normal 5.0 28.9

0.30 Normal 2.5 31.3

0.43 Inverted 12.0 27.2

0.38 Flattened 1.0 30.7

0.53 Normal 2.5 31.7

0.45 Flattened 6.0 26.8

0.42 Normal 3.5 32.3

0.58 Flattened Absent 23.8

0.77 Normal 8.0 31.1

0.53 Normal 2.0 33.2

0.45 Normal 3.0 32.3

0.58 Normal 17.0 26.5

0.52 Inverted 9.0 30.0

0.70 Inverted 6.5 30.8

0.40 Normal 1.0 33.5

0.59 Normal 2.5 32.1

0.61 Inverted 10.0 27.7

0.60 Normal 5.5 30.3

0.37 Normal Absent 34.0

0.32 Normal Absent 34.6

0.34 Normal Absent 34.9

0.36 Normal Absent 34.4

0.40 Normal Absent 34.2

0.37 Normal Absent 33.9

ricular block.

Table 2

Clinical causes of J waves in ECG

Proposals of J-wave classification in ECG

I J wave of hypothermia

II J wave in normothermic patients:

IIa Hypercalcemia

IIb Central nervous system lesion: subarachnoid hemorrhage,

after cardiac arrest and in dysfunction of the cervical

sympathetic system

IIc Rarely in early repolarization syndrome

IId Brugada bentitiesQ:IId1 Familial cases (617%): true Brugada disease

IId2 Sporadic cases (663%): Brugada syndrome

IId3 Acquired forms: those entities or clinical pharmacologic

conditions, where the Brugada phenotype or Brugada-type

ECG may be found as a consequence of promoting increase

in Ito channel function in the ventricular epicardium or decrease

in the slow calcium channel.

IIe In the cancelled forms of right ventricle arrhythmogenic dysplasia

IIf In Prinzmetal’s variant angina.

D. de Souza et al. / Journal of Electrocardiology 40 (2007) 47–52 51

latter, although widely used, constitutes an unjust designa-

tion because the first to describe it was Tomaszewski12 in

1938, and 5 years later, Grosse-Brockhoff and Schoedel13 in

Germany. Osborn’s14 boriginalQ description appeared only

15 years later. Ironically, highly regarded cardiology text-

books call the J-wave Osborne wave, adding the vowel e to

the original name of the author.15

The J wave is characteristic but not pathognomonic of

hypothermia because it may be observed in conditions of

normothermia.16,17

Experimental studies indicate that the appearance of Jwave

is a consequence of the presence of a transmural gradient in

the width of the ventricular wall, secondary to the existence of

a significant notch in phase 1 mediated by a greater activity

and/or density of the transient outward potassium current.

This greater I to channel activity and/or density in the

epicardial but not endocardial cardiomyocytes is responsible

for the characteristic aspect of the AP known as spike-and-

dome configuration of the AP. In addition, the greater initial

potassium outflow from the epicardium, as comparedwith the

endocardium, promotes a shortening of phase 2 in the

epicardium conditioning a transmural dispersion of repolar-

ization and appearance of J wave that, brought to a certain

level, gives rise to a higher tendency of ventricular arrhythmia

emergence by a mechanism called phase 2 reentry.18

Experimental cooling of the right ventricle outflow tract

in the dog in vivo mimics the electrophysiologic changes

that occurred in Brugada syndrome, leading to the appear-

ance of J wave secondary to Ito channel activation and

promoting the classic spike-and-dome configuration in the

AP of right ventricle outflow tract epicardial cells.19

Several entities are associated with the appearance of

J wave20 (J-wave syndromes, Table 2), which include,

among others, early repolarization syndrome (rare),21

variant angina,22 intoxication by tricyclic antidepressants,23

cocaine abuse,24 hypercalcemia,25 encephalic lesion,26

Brugada syndrome,27 idiopathic ventricular fibrillation such

as J waves prominent in the inferior wall,28 and the so-called

concealed forms of arrhythmogenic ventricular dysplasia.29

Experimental evidence supports the hypothesis that the

heterogeneous Ito channel distribution in the width of the

ventricular wall is responsible for the spike-and-dome–type

configuration of the AP of the epicardium and prominent

notch in phase 1 and shortening of phase 2 resulting in a

voltage gradient, which is expressed by the J wave.30

Hypothermia is 1 of the 3 causes of chronic metabolic

bradycardia, the other 2 being obstructive jaundice (due to

the bradycardic effect of biliary salts on the SA node) and

hypothyroidism. Sinus bradycardia is observed in the so-

called exhaustion effect of hypothermia where core temper-

ature is between 328C and 288C. This phase corresponds tomoderate hypothermia. In this phase, chills cease, muscle

rigidity appears, pain sensation to cold disappears, and

acidosis emerges (secondary to respiratory insufficiency and

microcirculation failure) with diminution in the respiratory

quotient from 0.82 to 0.65 at 308C, and there is superficial

and slow respiration with progressive bradycardia.

In hypothermia, the QT interval is prolonged in most

cases as a consequence of an extra wave at the site of the

J point and slowing of ventricular repolarization. In all

cases, the widening of the electric systole is reversible with

reversion of hypothermia.31

The T wave is found changed in a direct way according

to the degree of hypothermia. When J wave starts to be

of high voltage, concomitantly, the T wave of the corre-

sponding lead is inverted.

T waves with changes in polarity or of the axis are called

T-wave alternans and are observed during quick blood

transfusion in surgical hypothermia.32 Flattening asymmet-

ric inversion mainly in the anterior wall is described.

Hypothermia is associated with the presence of a higher

incidence of several arrhythmias, both supraventricular and

ventricular. Atrial fibrillation is described as an arrhythmia

with a significant incidence in moderate hypothermia, in

some series being observed in up to 50% to 60% of

the cases.33

In our material, it was evidenced in only 2 patients who

presented mild hypothermia. These differences regarding

atrial fibrillation found in the several series of literature are

related to the heterogeneous nature of the studied popula-

tions. The elderly present a higher prevalence of atrial

fibrillation. Thus, regarding the mean age of 37.2 years of

our patients, the sample represents a young population with

a much lower natural tendency to atrial fibrillation.

Idioventricular rhythm, barely reported in literature, was

present in 6 patients; in 5 cases, hypothermia was severe.

Probably, the absence of automatic supra-His activity

allowed a low escape focus to be the only form to maintain

electric command. Appearance of junctional rhythm is also

related to decreased conduction.

Total atrioventricular block is little reported in literature

and is related to decrease in conduction of the stimulus

released by cold. It is an adverse situation where the

insertion of any type of device (such as a pacemaker cable)

that would be in contact with the hypothermic heart could

release ventricular fibrillation. Significant arrhythmias did

not appear with body temperatures above 328C. This is whythis limit of moderate hypothermia is induced for therapeu-

tic reasons.34

D. de Souza et al. / Journal of Electrocardiology 40 (2007) 47–5252

Limitations

The electrocardiographic modifications found are not

necessarily and exclusively caused by hypothermia. Take into

account that a high number of patients were people with an

advanced degree of drunkenness or in use of antiepileptic

drugs that may have influenced the ECG. Because this is a

mixed populationwith regard to etiology, we de not know how

many factors such as drugs influenced the observations. This is

particularly true for rhythm disturbances and ECG intervals.

This is a merely descriptive article on ECGs in patients at the

moment in which their central temperatures are equal to or

lower than 358C, and in absence of metabolic or electrolytic

disorders, determined by laboratory through electrolyte dosage

and gasometry. This issue is very important. Nevertheless, in

the review of the databases, a history of prior use of drugs was

not found, and these details were ratified in interviews with the

relatives of the patients. Thus, although we cannot state

irrefutably that there were no drugs interfering with the

analysis of the electrocardiogram, we think it is quite unlikely

that this factor may be altering the comprehensive interpreta-

tion of the electrocardiographic tracings.

Conclusion

Electrocardiographic changes in accidental hypothermia

are frequent and characteristic, and in many cases, may be

the diagnostic clue in patients with conscience deficit in

emergency units, even in patients from a tropical climate

where the population at risk may be exposed to temperatures

below 208C.

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