Abstract

Moderate pre-cordial mechanical impact can cause sudden cardiac death, even in the absence of morphological damage to the heart. This is the most severe expression of a condition termed, in the 19th century, Commotio cordis. Experimental studies performed in the early 1930s showed that sudden cardiac death after chest impact is brought about by an intrinsic cardiac response to the mechanical stimulus. The precise (sub-)cellular mechanisms of this response are still poorly understood. This article summarises experimental findings on the condition and relates them to the more recently established concept of cardiac mechano—electric feedback. As a result, an explanation of the mechanisms that give rise to sudden cardiac death by Commotio cordis and targets for further research are suggested.

Time for primary review 26 days.

1 Introduction

Non-penetrating mechanical impact to the pre-cordial chest can cause serious dysrhythmia, even in the absence of any microscopic damage to the heart or other organs of the chest. This setting is termed Commotio cordis (Latin: ‘disturbance of the heart’) and refers to cardiac concussion or the result thereof, including sudden cardiac death (SCD).

It is important for the understanding of this condition to distinguish it from blunt pre-cordial impact that is accompanied by cardiac bruising [1]. The latter is called Contusio cordis (Latin: ‘bruising of the heart’) and has been described as early as 1763 [2].

Commotio cordis has recently seen an impressive surge in publicity via print and electronic media and has become a concern of amateur and professional athletes, sports and consumer organisations, legislation and jurisprudence, as well as clinical and fundamental bio-medical research. This recent publicity is fuelled by reports of SCD in young, healthy athletes after relatively minor mechanical impact to the chest, usually by projectiles like baseballs or pucks (Fig. 1).

Contrary to popular belief, Commotio cordis is not a new phenomenon. Early case reports of SCD by Commotio cordis can be traced back by over 120 years [4,5], and by the late 19th century both the term and the concept of Commotio cordis were well established (for a historic account see Ref. [6]). The classic concept of Commotio cordis was not one of a necessarily lethal condition. It included a variety of clinical manifestations ranging from transient, self-rectifying rhythm disturbances, over various chronic cardiac conditions, to SCD immediately after mechanical impact [7–11].

Fig. 1

Schematic representation of the location of impact sites, sustained during various sports activities, that led to sudden cardiac death by Commotio cordis. From [3] with permission.

Fig. 1

Schematic representation of the location of impact sites, sustained during various sports activities, that led to sudden cardiac death by Commotio cordis. From [3] with permission.

This review will summarise early and contemporary experimental insight into Commotio cordis, suggest mechanisms that give rise to SCD after moderate pre-cordial impact, and identify targets for further research.

2 Early experiments: development of the vascular crisis concept

The first experimental studies that shaped the concept of Commotio cordis were performed by Felice Meola in the 1870s [4]. He reported that mechanical stimulation of the chest of rabbits (details of mechanical stimulation and observed functional parameters are not given) could cause instant cardiac death, which he attributed to a ‘profound vagal reflex’. This theory dominated the interpretation of SCD by Commotio cordis for the next half century [1,7–9,12].

Investigations into the cause and mechanisms of Commotio cordis, conducted in the 1930s by Georg Schlomka and colleagues at Bonn University, led to a re-assessment of the underlying mechanisms. In a series of six reports [13–18] they published the findings of more than 800 experiments on anaesthetised rabbits, cats and dogs that were subjected to various forms of moderate pre-cordial mechanical stimulation. This included precordial thumping using mechanical probes (wooden hammers or rubber-edged metal reflex probes) of varying weight (20–260 g) and contact area (1–20 cm2), as well as slow compression, or vigorous agitation of the chest. Patho-physiological effects of mechanical stimulation were judged from recordings of the ECG, respiration, arterial and central venous pressures.

On the basis of these experiments, Schlomka established the intrinsic nature of the condition, and identified three principal determinants of the severity of cardiac rhythm disturbances after moderate chest impact [8]:

  • type of mechanical stimulus,

  • strength of impact,

  • impact site.

2.1 Intrinsic nature of Commotio cordis

In experiments with bi-lateral vagotomy or application of atropine Schlomka and colleagues did not observe any effect on either incidence or character of arrhythmias after pre-cordial impact. This disproved the previously held ‘profound vagal reflex’ theory [1,4] of Commotio cordis.

2.2 Type of mechanical stimulus

Swift, impulse-like mechanical stimulation of relatively small pre-cordial areas (4–5 cm2) was found to be most arrhythmogenic. In contrast, slow compression or violent shaking of the chest were ineffective in triggering arrhythmias. Also, larger contact areas reduced arrhythmogeneity.

2.3 Strength of impact

Serious rhythm disturbances were most frequently observed when medium to high forces (probes weighing 50–125 g) were applied. Lighter probes (20 g) did not cause lethal rhythm disturbances, while heavier ones (260 g) usually lead to elements of cardiac bruising which, by definition, does not constitute Commotio cordis.

In this context, Schlomka commented on the relevance of mechanical buffer properties afforded by the plasticity of the chest (small animals are more likely to show mechanically-induced dysrhythmia than larger ones), the role of direct mechanical coupling of impact site and cardiac muscle (larger animals show next to no arrhythmia if impacted in supine position when the heart is relieved of its intimate contact with the anterior chest wall), and the potential of protective gear to reduce the incidence of arrhythmias (like boxing gloves that increase impact area and act as an additional mechanical buffer).

2.4 Impact site

Schlomka and colleagues established a close correlation between impact site and electrophysiological effect. Atrio-ventricular conduction disturbances, for example, were most frequently observed upon mechanical stimulation near the upper or medium sternum, while ventricular fibrillation (VF) occurred exclusively when the stimulus was applied close to the medium to lower sternum. Impact near the location of the cardiac apex predominantly caused ectopic beats and/or ventricular tachycardia (VT), while mechanical stimulation of the chest or abdomen distant from the pre-cordium did not result in arrhythmogenesis.

From this data the authors concluded that the effects of Commotio cordis are caused by direct mechanical impulse transmission to the heart, and that the mechanisms involved are inherently intra-cardiac. As ECG recordings and histological samples frequently showed tell-tale signs of myocardial ischaemia, they suggested that mechanical stimulation causes coronary vasospasms [8]. SCD by Commotio cordis was explained by acute constriction of cardiac vessels, termed ‘vascular crisis’.

3 Contemporary experiments: limits of the vascular crisis concept

While the mechanical induction of localised myocardial ischaemia, proposed by Schlomka, would be a potent cause for more slowly occurring clinical manifestations of Commotio cordis, it is hard to see how a mechanism that is based on metabolic pathways could cause instantaneous VF upon pre-cordial impact (see, for example, Fig. 2). Furthermore, recent experimental findings, obtained in a porcine model of Commotio cordis, show that — even in cases where ST segment elevation is observed on the ECG — coronary perfusion abnormalities cannot usually be confirmed angiographically [19]. It is unlikely, therefore, that mechanically-induced SCD may satisfactorily be explained by coronary vasospasms alone; an alternative mechanism must be involved in this response.

The first indications of the nature of this alternative mechanism were derived in the 1980s from experiments that identified a fourth principal determinant of the arrhythmogeneity of pre-cordial impact [20]:

  • impact timing relative to the cardiac cycle.

Fig. 2

ECG (lead I, top) and left ventricular pressure recording (LVP, bottom), obtained from an anaesthetised pig, subjected to a pre-cordial impact that coincided with the upstroke of the T-wave. Note the swiftness of mechanical induction of VF and loss of contractility (within one cardiac cycle). From [19] with permission.

Fig. 2

ECG (lead I, top) and left ventricular pressure recording (LVP, bottom), obtained from an anaesthetised pig, subjected to a pre-cordial impact that coincided with the upstroke of the T-wave. Note the swiftness of mechanical induction of VF and loss of contractility (within one cardiac cycle). From [19] with permission.

Moderate precordial impact is particularly effective in triggering instant VF if delivered during the early T-wave of the ECG (Fig. 2). This timing is identical to the ‘vulnerable period’ for electrical induction of VF (identified in 1936 [21,22]) and poses questions as to what mechanism would: (i) allow near-instantaneous translation of a mechanical stimulus into an electrophysiologically relevant signal that is (ii) powerful enough to cause serious rhythm disturbances and that is, (iii) particularly potent in doing so during the T-wave.

Obviously, the above set of questions might be ill-posed, as the link between the timing of a mechanical impact and its electrophysiological effect may be primarily related to the mechanical, rather than the electrical cycle of the heart.

One could imagine, for example, that the extent of background tissue strain and/or dimensions of the cardiac chambers would determine susceptibility to mechanical induction of VF. Maximum filling of the ventricles coincides with the PQ segment, however, so this would not explain the observed peak sensitivity to mechanical induction of VF during the T-wave.

Alternatively, intra-ventricular hydrostatic pressures and tissue stress might determine mechanical impulse transmission and, hence, arrhythmogeneity. If this were the case, one would expect little or no effect of mechanical stimulation in relaxed cardiac muscle. Both experimental and clinical observations, however, show that mechanical stimulation of the diastolic heart is a very effective means of triggering ectopic beats [23–25].

Furthermore, a link to tissue stiffness would suggest that the most severe rhythm disturbances (that would, perhaps, also be most potent in affecting the cardiac conduction system in deeper layers of the myocardium) should occur during peak contraction, covering a period of time beginning prior to and extending beyond the end of the T-wave (see also Fig. 2). As illustrated in Fig. 3, however, mechanically-induced disturbances in impulse conduction occur upon mechanical stimulation applied as early as during the QRS complex, i.e. prior to notable ventricular contraction. Furthermore, the timing of peak susceptibility to mechanical induction of VF has recently been narrowed down to a time window of 10–15 ms during the upstroke of the T-wave [19]. This period is too brief to be satisfactorily explained on the basis of the more slowly occurring changes in cardiac mechanics.

Fig. 3

Schematic representation of the effects of pre-cordial mechanical stimulation on cardiac rhythm. Labels above the ECG pattern illustrate the number and timing of interventions; markers below denote the type and number of rhythm disturbances caused. Key: CHB, complete heart block; ST↑, ST segment elevation; LBBB, left branch bundle block; VF, ventricular fibrillation; NSVT, non-sustained ventricular tachycardia. From [3] with permission.

Fig. 3

Schematic representation of the effects of pre-cordial mechanical stimulation on cardiac rhythm. Labels above the ECG pattern illustrate the number and timing of interventions; markers below denote the type and number of rhythm disturbances caused. Key: CHB, complete heart block; ST↑, ST segment elevation; LBBB, left branch bundle block; VF, ventricular fibrillation; NSVT, non-sustained ventricular tachycardia. From [3] with permission.

Thus, while the mechanical state of the heart will undoubtedly affect its response to mechanical stimulation, there does not appear to be a simple correlation of type and severity of electrophysiological changes with either background ventricular pressure or volume.

On the other hand, the timing of the ‘vulnerable window’ for mechanical induction of VF coincides with early repolarisation of the ventricles. The vulnerability of the heart to electrical induction of VF during this period is known to be unusually high, since it is the time during which different regions of the heart show varying levels of membrane repolarisation and, hence, refractoriness, electrical load and excitability. Supra-threshold stimulation during that time is able to trigger action potentials in discrete volumes of cardiac tissue only. This, together with pronounced and highly dynamic gradients in refractoriness and electrical load, is believed to be key to the induction of VT and VF [26–28].

While the timing of peak inducibility of VF has predominantly been studied using electrical stimulation, there is no reason to assume that the situation is much different in the case of mechanical perturbation as — via mechano—electric feedback (MEF) — mechanical stimuli may be: (i) transformed instantaneously into (ii) (patho-)physiologically relevant electrical signals of (iii) significant arrhythmogeneity [29]. Thus, MEF may provide answers to the above set of questions regarding the mechanisms underlying mechanically induced SCD.

4 Prospects: the cardiac mechano—electric feedback concept

Cardiac electrical and mechanical activity are closely interrelated and affect each other directly, even on the level of single cardiac cells, via the cross-talk of excitation—contraction coupling and MEF (for reviews see Refs. [30–32] and Babuty and Lab [33], this issue).

A major mechanism of MEF is stretch—activation of specialised, mechano-sensitive ion channels that increase their open probability in response to direct membrane deformation. On the basis of their ion selectivity one can distinguish at least two major groups of cardiac stretch-activated channels: K+-selective (with a reversal potential near the resting potential of cardiomyocytes) and cation-selective channels (reversal potential between −20 and 0 mV [34–36]).1

Their properties and potential role in mechanical induction of cardiac arrhythmia has been the subject of fundamental research since their discovery in cardiac cells about a decade ago [40,41]. The effects of stretch-activated channels on cardiac electrophysiology depend on both amplitude and timing of the mechanical stimulus. Thus, diastolic stretch tends to cause membrane depolarisation, while systolic stretch primarily affects the shape and time—course of action potential repolarisation (see also Fig. 4A).

4.1 Diastolic stretch

The depolarising effect of diastolic stretch has been demonstrated in isolated ventricular cardiomyocytes [42] and pacemaker cells [43], ventricular [29] and pacemaker tissue [44], as well as in whole heart preparations [45].

If the applied mechanical stimulus is sufficiently large, it may trigger premature ventricular excitation [45] or runs of VT [46] in isolated heart preparations. This response is usually attributed to stretch-activated cation-selective channels, since their direct activation is sufficient to trigger action potentials in isolated cardiac myocytes [47]. Furthermore, their pharmacological blockade in isolated heart preparations is sufficient to prevent stretch-induced atrial fibrillation [48] and generation of mechanically induced ventricular ectopic beats [49].

This depolarising component of mechanical stimulation is so pronounced that pre-cordial mechanical impact has had a long history of clinical use for resuscitation, serving as a mechanical pacemaker during asystole [23] or as a mechanical stimulator/defibrillator in VT and VF [50–53]. Interestingly, the ideal location for triggering a (desirable in the context of resuscitation) single ectopic beat appears to be medial of the apex [54] — a region also identified by Schlomka as not likely to promote mechanical induction of VF [8]. Energy levels as low as 0.04–1.5 J were found to effectively trigger single ectopic beats in man without causing VT, even if mechanical stimulation was timed to coincide with the vulnerable window [54]. The typical energy levels that do cause mechanically-induced VF (130–300 J, as calculated from average projectile speed and mass, reported for cases of SCD after baseball injuries [3] or in vivo animal experiments [19]) are two to three orders of magnitude higher, suggesting that optimally performed mechanical cardioversion may be a much safer procedure than commonly assumed.

Fig. 4

(A) Patch clamp recording of an isolated cardiac myocyte before (control, dark curve) and during (stretch, light curve) application of axial stretch (10% of resting length). Note the stretch-induced diastolic depolarisation and the afterdepolarisation-like changes in repolarisation. From [58] with permission. (B) Monophasic action potential recordings from right endocardium in a patient undergoing pulmonary valvuloplasty. Top: control. Bottom: response to acute obstruction of right ventricular outflow tract, resembling early afterdepolarisations (slanted arrow), from which premature beats arise (upward arrows). From [60] with permission.

Fig. 4

(A) Patch clamp recording of an isolated cardiac myocyte before (control, dark curve) and during (stretch, light curve) application of axial stretch (10% of resting length). Note the stretch-induced diastolic depolarisation and the afterdepolarisation-like changes in repolarisation. From [58] with permission. (B) Monophasic action potential recordings from right endocardium in a patient undergoing pulmonary valvuloplasty. Top: control. Bottom: response to acute obstruction of right ventricular outflow tract, resembling early afterdepolarisations (slanted arrow), from which premature beats arise (upward arrows). From [60] with permission.

4.2 Systolic stretch

The effects of systolic stretch on electrophysiology are less clear-cut. A whole range of changes, primarily in action potential repolarisation, have been observed, including both shortening [55] and prolongation of the action potential [56], as well as cross-over of the repolarisation curve [57]. Furthermore, axial stretch of isolated cardiomyocytes may cause early afterdepolarisation-like events (Fig. 4A, [58]), which could underlie similar responses in multicellular experimental preparations [45,59] and man [60]. These mechanically induced afterdepolarisations have been linked to premature ventricular contraction in patients (Fig. 4B).

Regarding the (sub-)cellular mechanisms involved in the genesis of VF during Commotio cordis, there is little direct experimental information. Recent data, obtained in whole animal studies, imply a role for the ATP-dependent K+ (K+ATP) channel [61]. In that study the incidence of VF upon systolic pre-cordial impact (observed during a 10–15 ms time window preceding the peak of the T-wave) was significantly reduced by application of glibenclamide, a non-specific [62,63] inhibitor of the K+ATP channel. Also, the average extent of ST segment elevation (observed after mechanical stimulation between the Q and T waves, see Fig. 3) showed a pronounced glibenclamide-related reduction [61].

While the cardiac K+ATP channel is not perceived to be a classic ‘stretch-activated ion channel’, it is known from earlier patch—clamp experiments that the open probability of that channel is increased by stretch [64].2

2

As with the other ion channel classifications, there are examples of ‘overlapping properties’, like combined voltage and ligand dependent activation of channels.

Accordingly, K+ATP channels have been found to provide a hyperpolarising effect on isolated cardiac cells during stretch [65]. Furthermore, mechanical and ischaemic activation of K+ATP channels have been reported to act co-operatively [66]. This could help to explain why K+ATP channel-related mechanisms appear to be involved in both stretch-induced and ischaemic pre-conditioning [67], and how mechanical prevention of ‘ischaemic bulging’ may help to reduce extracellular K+ accumulation in the ischaemic zone [68].

These findings could also help to explain why some of the changes in ECG parameters after Commotio cordis (like ST segment elevation) mimic those commonly associated with myocardial ischaemia, even when there does not appear to be significant disturbance of coronary flow, and why application of glibenclamide reduces ST segment shift after pre-cordial impact.

With regard to the beneficial effect of blocking K+ATP channels on the incidence of stretch-induced VF, however, the situation is more complex. Given the channel's ion selectivity, its reversal potential is near the diastolic membrane potential of ventricular cells. The effect of a transient stretch-induced increase in K+ATP channel open probability during early ventricular repolarisation will, therefore, vary across the ventricular wall, depending on the actual membrane potential in cells of different regions.

Cells that are already fully repolarised will be least affected, as there would be hardly any voltage difference between cell membrane potential and K+ATP channel reversal potential (thus not providing a notable driving force for directional ion movement through the channel, even if the channel's open probability was increased during mechanical stimulation).

On the other hand, cells that are still depolarised would be subject to a repolarising current. Since the degree of ventricular repolarisation during early T-wave covers the whole range of membrane potentials — from late action potential plateau to resting membrane potential levels — stretch—activation of K+ATP channels would have regionally differing electrophysiological effects and disturb the normal pattern of refractoriness, load and excitability. This illustrates why transient activation of K+ATP channels during early repolarisation may be pro-arrhythmic, despite the potential anti-arrhythmic effect of sustained pharmacological activation of potassium channels [69], as the latter reduces action potential duration throughout the myocardium, not just in sub-populations of incompletely repolarised cells.

Furthermore, the local mechanical effect of a pre-cordial impact will not be distributed homogeneously throughout the heart. Accordingly, the extent of stretch-activation of K+ATP channels will vary across the myocardium.

Finally, it is not inconceivable that the expression levels of the K+ATP channel vary in different regions of the heart, as has been observed for many other potassium channels in mammalian myocardium [70].

Thus, it can be seen how, during early repolarisation, a transient mechanically-induced increase in open probability of cardiac K+ATP channels (or other, K+-selective stretch-activated channels, for that matter) could increase electrophysiological tissue heterogeneity and therefore contribute to VT and/or VF. This heterogeneity would be diminished by application of pharmacological blockers of mechanically-modulated potassium channels, reducing the heart's ability to sustain VT or VF. What is more difficult to see, though, is how activation of potassium channels would provide the trigger for ectopic excitation which is so frequently observed upon mechanical stimulation of the heart [25], and which is understood to be required for the immediate induction of VT or VF (see Fig. 2, VF starts before the next wave of regular excitation occurs).

Excitation can obviously be triggered only in cells that have at least partially re-gained excitability, and may only be caused by activation of ion channels with a reversal potential that is more positive than the threshold potential for action potential generation.3

3

Alternatively, stretch-induced reduction of a ‘hyperpolarising’ current could depolarise cells in the presence of a significantly large ‘depolarising’ background current component. This is thought to be a less likely scenario in the mammalian heart, where stretch-inactivated ion channels have not yet been demonstrated.

In the context of mechanically-induced excitation, the most probable candidate for this response is the aforementioned stretch-activated cation-selective channel.

The potential electrophysiological effects of mechanical activation of cation-selective channels during early repolarisation are illustrated in Fig. 5 and could range from changes in action potential repolarisation in cells that are still depolarised (panel A), over the induction of early and delayed afterdepolarisation-like behaviour (panels B and C) to the induction of ectopic excitation (see also Fig. 4B).

The contribution of a particular ion channel population to (patho-)physiological responses would, obviously, best be assessed in vivo using pharmacological blockers of the channel. Until recently, most studies used Gadolinium, a rather non-specific blocker of stretch-activated cation-selective channels [72,73]. Gadolinium furthermore precipitates almost completely in bicarbonate-buffered solutions [74,75], which renders it of little use for in vivo studies. Such studies, however, have become possible now as a new selective, high-affinity peptide blocker of stretch-activated cation-selective channels has been isolated from the Grammostola spatulata spider venom [76]. In experiments on isolated hearts, this peptide has already been shown to be highly efficient in preventing stretch-induced atrial fibrillation [48].

Thus, blocking the (mechano-sensitive) K+ATP channel has been reported to reduce the incidence of VF after moderate pre-cordial impact. This is probably achieved by preventing the heart from developing arrhythmia-sustaining mechanisms like a mechanically-induced increase in tissue inhomogeneity (including parameters like excitability, refractoriness and electrical load). The nature of the trigger mechanism of VT or VF during Commotio cordis remains to be validated. The available experimental and clinical information is consistent with a contribution of MEF, acting via stretch-activated cation-selective channels.

5 Open questions

Further experimental investigations into the cause and (sub-)cellular mechanisms of Commotio cordis-related disturbances in cardiac electrophysiology are required and should address a range of questions, including those listed below.

Fig. 5

Schematic representation of the potential arrhythmogenic effects of mechanical activation of cation-selective channels during early repolarisation (upstroke of the T-wave, see top ECG trace). Effects would depend on the actual membrane potential of cardiomyocytes in different regions of the heart (panels A—C) and could include: (A) changes in action potential duration, including shortening [55], prolongation [56], or cross-over [57] of the repolarisation curve [71]; (B) early afterdepolarisation (EAD) like behaviour; or (C) delayed afterdepolarisation (DAD) like events. Both early and late afterdepolarisations are known to be capable of triggering ectopic excitation, as observed in experimental models and patients [45,59,60].

Fig. 5

Schematic representation of the potential arrhythmogenic effects of mechanical activation of cation-selective channels during early repolarisation (upstroke of the T-wave, see top ECG trace). Effects would depend on the actual membrane potential of cardiomyocytes in different regions of the heart (panels A—C) and could include: (A) changes in action potential duration, including shortening [55], prolongation [56], or cross-over [57] of the repolarisation curve [71]; (B) early afterdepolarisation (EAD) like behaviour; or (C) delayed afterdepolarisation (DAD) like events. Both early and late afterdepolarisations are known to be capable of triggering ectopic excitation, as observed in experimental models and patients [45,59,60].

  • What is the (sub-)cellular trigger mechanism of Commotio cordis-related rhythm disturbances? The mechanisms that give rise, in particular, to mechanically-induced VF in vivo require experimental elucidation, ideally using selective blockers of the cation-selective stretch-activated ion channel.

  • What is the influence of cardiac mechanical properties on the electrophysiological effects of mechanical stimulation? Commotio cordis-type mechanical impacts should be studied in vivo during different phases of the mechanical cycle and during pressure/volume overload to correlate electrophysiological effects, such as the extent of ST segment elevation, with the cardiac mechanical environment. Also, the precise lag-time between chest impact and its effect on the heart, reported to be between 5 ms and 40 ms [20,77,78], warrants further elucidation.

  • Does the vulnerable time window shift during pharmacological interventions? Under the influence of drugs (like K+ATP channel blockers), peak susceptibility to mechanical stimulation could shift outside the target observation period established in control experiments (in particular if this period is as brief as 15 ms). This could lead to false—negative findings and invalid leads for data interpretation and should be assessed in vivo.

  • Can Commotio cordis be reproduced in vitro? Current isolated heart models allow mechanical induction of atrial fibrillation, ventricular ectopic excitation, and runs of VT. Mechanically-induced VF has less frequently been observed in isolated hearts and was generally accompanied by structural damage to the myocardium [79]. In order to study the mechanisms of SCD by Commotio cordis in controlled ex vivo settings, commotional induction of VF should be reproduced in isolated hearts and assessed in relation to the cardiac electrical and mechanical cycles.

  • What are the mechanisms of the more slowly occurring consequences of Commotio cordis? The possible links between post-commotional complications (like ST segment elevation, conduction abnormalities, ventricular dilatation, etc.) and mechanical effects on capillary micro-circulation and sub-microscopic tissue integrity, gene expression and protein synthesis [80–82] or other (patho)physiological mechanisms warrant further elucidation.

6 Conclusions

Commotio cordis is not a new phenomenon. For well over a century it was understood to be a response of the heart to pre-cordial impact, causing cardiac concussion and leading to serious rhythm disturbances, including SCD, in the absence of structural damage that would appear severe enough to explain the observed electrophysiological effects.

There are at least four risk factors that determine the severity of mechanically-induced dysrhythmia:

  • type of mechanical stimulus: swift, impulse-like impact to small contact area,

  • strength of impact: medium to high sub-contusion levels,

  • impact site: pre-cordial area with emphasis on the ventricular projection,

  • impact timing relative to cardiac cycle: early T-wave.

SCD by Commotio cordis is a relatively rare event. This is, in all likelihood, due to the fact that seldom all four risk factors are present at the same time. Knowledge of risk factors should also aid prevention of accidental Commotio cordis (design of sports equipment, protective gear) and allow optimisation of procedures for mechanical pacemaking and resuscitation (which appear to be based on similar, if not identical mechanisms [32]) by optimising the location and force of mechanical stimulation, as well as by synchronising its application with the QRS complex.

The underlying mechanisms of cardiac rhythm disturbances caused by Commotio cordis are likely to include cardiac MEF and elements of myocardial ischaemia. The latter may give rise to some of the more slowly developing consequences of Commotio cordis. Instantaneous effects of mechanical stimulation on cardiac electrophysiology, such as SCD by Commotio cordis, may be explained by cardiac MEF. In this context, mechanical activation of cation-selective channels could provide a trigger mechanism, while K+-selective channels might contribute to arrhythmia-sustaining processes by increasing electrophysiological tissue heterogeneity. Further studies are required to verify the precise sub-cellular processes that give rise to both trigger and sustaining mechanisms of serious dysrhythmias after moderate, non-penetrating impact to the chest.

Acknowledgements

The authors acknowledge valuable contributions to this review by Patrizia Camelliti, Alan Garny and Long Xian Cheng. The Oxford Cardiac MEF Group is supported by grants from the British Heart Foundation and the Medical Research Council, London. P.K. is a Royal Society Research Fellow.

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Author notes

1
Another group of ion channels, frequently assumed to be mechano-sensitive, is constituted by cell volume-activated channels. These channels tend to be selective for either Cl or K+. Contrary to stretch-activated channels, they require an increase in cytosolic volume for their activation and are not usually affected by direct stretch. They are unlikely, therefore, to form a major substrate for Commotio cordis-induced changes in cardiac electrophysiology. For more detail see the reviews in Refs. [37–39].