The Impacts of The Earthquake on The Cardiovascular System

Özge Turgay Yıldırım, Demet Laflı Tunay, Ayşegül Turgay

Volume 7 · Issue 2 · pp. 59–63

Received: 20230324  Accepted: 20240613  Published: 20240630

Abstract

Aim: Various physiological and psychological effects of earthquakes can be seen on the human body, even without a direct physical impact from the earthquake. Both the experience of the earthquake process and the earthquake-related subsequent life changes cause stress through the activation of the sympathetic and parasympathetic systems in the body. This stress can affect various physiological processes, including the cardiovascular system. In this review, the effect of earthquakes on the cardiovascular system was aimed to be discussed in line with the available evidence. Discussion: There are studies showing that natural events such as earthquakes increase the incidence of adverse cardiac events, such as myocardial infarction, heart failure, hypertension, and sudden cardiac death, or cause existing cardiac diseases to worsen during these periods. However, there are also some evidences with conflicting results. Therefore, the effect of earthquakes on cardiovascular diseases has not been clearly demonstrated yet. Conclusions: Even survivors of earthquakes without physical injury are exposed to stress secondary to both internal and external factors. Studies indicate that individuals who are involved in the earthquake process may have adverse effects on cardiovascular health in the short and long term. Therefore, it is important to take necessary precautions and create appropriate conditions, especially in people with cardiovascular disease..

Keywords: Earthquake, myocardial infarction, hypertension, sudden cardiac death.

Introduction

The phenomenon of shaking the surface of the Earth through which the vibrations that occur suddenly due to fractures in the earth's crust spread as seismic waves is called an earthquake. Earthquake is an unavoidable natural event.1 Since the formation of the world, earthquakes have occurred consecutively in seismically active regions, resulting in the destruction of millions of people and their shelters. Even if individuals who have experienced the earthquake process survive the process without physical injury, it is inevitable that there will be psychological effects. These individuals have to cope with the injuries and deaths of not only their families but also their friends and relatives, and they have to stay in emergency shelters and small-scale temporary housing or their relatives' homes for days or months.2 For these reasons, individuals experiencing the earthquake process are exposed to acute and subacute psychological stress.3

Corresponding Author: Özge Turgay Yıldırım, ozgeturgay@gmail.com, Received: 24.03.2023, Accepted: 13.06.2024, Available Online Date: 30.06.2024 Cite this article as: Yıldırım ÖT, Tunay DL, Turgay A. The Impacts of The Earthquake on The Cardiovascular System. J Cukurova Anesth Surg. 2024; 7(2): 59-63.

https://doi.org/10.36516/jocass.1270533 Copyright © 2024 This is an open access article distributed under the terms of the Creative Commons Attribution-Non-Commercial-No Derivatives License 4.0 (CC-BY-NC-ND), where it is permissible to download and share the work provided it is properly cited. The work cannot be changed in any way or used commercially without permission from the journal.

Stress affects the autonomic nervous system, hypothalamus-pituitary-adrenal axis by causing an allostatic load in the body in the long term and this causes effects on the cardiovascular, metabolic and immune systems. Being exposed to constant stress also causes less or more activation in the allostatic system, leading to disruptions in body regulation.4 In other words, stress can harm the body by affecting the body physiology.5 The magnitude of the threat, or the severity perceived by the individual, determines the magnitude of the individual's stress response to internal or external challenges.4 Emotional or physical stress can affect acute and chronic diseases.6-10 Unexpected natural events such as earthquakes can cause cardiovascular events by causing acute, subacute and chronic stress.3 In this review, we aimed to compile the effects of the earthquake on the cardiovascular system.

Effect of earthquakes on acute coronary syndrome

Myocardial infarction is one of the most important causes of mortality and morbidity. In addition to well-known risk factors for myocardial infarction such as diabetes mellitus, hypertension, smoking, factors such as winter season, infections, physical exertion, insomnia and nervousness can also trigger myocardial infarction.11-14 Studies draw attention to the fact that unexpected natural events can also trigger myocardial infarction.15,16 There are conflicting results in studies investigating the relationship between earthquakes and acute coronary syndrome.

The Great East Japan Earthquake with a magnitude of 9.0 and subsequent tsunami on March 11, 2011, severely damaged the region. During this period, the incidence of acute coronary syndrome in Fukushima Prefecture was studied. While no increase was observed in the incidence of acute coronary syndrome in all districts in this study, an increase was observed in the incidence only in Iwaki district in the subgroup analysis.17 In a study conducted in patients with ST-elevation myocardial infarction in Iwate Prefecture, when the patients during the 2011 earthquake and the patients in the same time period in 2010 were examined, it was stated that there was no difference in the number of patients presenting with myocardial infarction, but the rate of percutaneous coronary intervention decreased and in-hospital mortality increased.16 Another study conducted in Miyagi Prefecture showed that acute coronary syndromes increased in the early period but tended to decrease after 2-3 weeks.18 Tanaka et al.19 reported that the incidence of acute coronary syndrome increased in the first 4 weeks after the earthquake and then returned to its normal course. This study also examined the aftershocks of the main earthquake and the incidence of acute coronary syndrome during this period. As a result, it was seen that there is a positive correlation between seismic scale and admissions due to acute coronary syndrome.19 In a single-center study by Nozaki et al.20, it was stated that there was a significant increase in patients with acute coronary syndrome who applied to the emergency department when compared to previous years. Again, another study conducted in Iwate Prefecture compared the years 2009-2010 before the earthquake with the earthquake period and afterwards until 2014, and in this study, the areas affected by the earthquake and tsunami were divided into high impact zone and low impact zone. In this study, the number of non-fatal myocardial infarctions did not change according to years in both the high impact zone and the low-impact zone. The number of fatal myocardial infarctions did not change over the years in the low-impact zone. However, while fatal myocardial infarction increased significantly in the high impact zone compared to the predisaster period, this significant difference continued in the following 2012-2014 years.21 In some studies conducted during the Hanshin-Awaji (1994), Athens (1981), The Noto Peninsula (2007) earthquakes, it was found that hospital admissions secondary to acute coronary syndrome increased after the earthquake.22-24 When the relationship between the Newcastle earthquake (1989) and the incidence of myocardial infarction was examined, a statistically significant increase was not found in terms of fatal and non-fatal myocardial infarction, although there was a numerical increase.25

Brown et al.26, in their study published with the hypothesis that the earthquake time and being awake or asleep may be important in acute coronary syndrome, compared the 1989 Loma Prieta and 1994 Northridge earthquakes; they suggested that the incidence of acute myocardial infarction when people were awake in the Loma Prieta earthquake at 05.04 pm was lower than the Northridge earthquake which occured at 04.31 am. A similar result was found in the Christchurch earthquakes. In the Christchurch earthquake, which happened at 4.36 am in 2010, the number of applications due to ST elevation myocardial infarction increased in the first two weeks, but a similar pattern was not found after the earthquake at 12.51 pm in 2011.27

The intense stress caused by earthquakes can activate the sympathetic system and the renin-angiotensin aldosterone axis, leading to myocardial damage and cardiac adverse outcomes. Sympathetic activity triggered by mental stress may trigger myocardial ischemia, especially in individuals with basal coronary artery disease.13,28 In addition, interrupting antiischemic or antiaggregant treatment may lead to an increase in the incidence of acute coronary syndrome in the early post-earthquake period, as patients using drugs for coronary artery disease may have problems in accessing the drug after the earthquake. In the long term, it can be expected that there will be a chronic stress environment in earthquake survivors as they lose their relatives and accommodation opportunities. Studies have shown that there is an increase in waist circumference, body-mass index, weight, Hemoglobin A1c levels, decrease in HDL levels, deterioration in physical activity, mental health and socioeconomic status, especially in those who had to relocate after the earthquake.2,29 Worsening of cardiovascular risk factors may also lead to increases in cardiovascular diseases in the long term.

Effect of earthquakes on congestive heart failure

When Nozaki et al.20 compared the congestive heart failure patients admitted to the emergency department in the 3-week period following the 2011 Great East Japan Earthquake with the number of patients admitted in the same weeks in 2009 and 2010, they found a significant increase in the number of patients presenting with this diagnosis after the earthquake. In their study, Aoki et al.18 showed that admissions to hospital with heart failure increased after the earthquake and that the applications entered a decreasing trend only in the 6th week of the event. Major events such as earthquakes can activate the sympathetic system and cause high blood pressure and heart rate.30,31 In addition, during this period, the habits of patients such as eating and salt intake change due to unsuitable conditions.18 In addition, during this period, it becomes difficult for patients with heart failure to access the drugs they regularly use. Apart from these, infectious diseases may increase due to the deterioration of accommodation opportunities, and the possibility of decompensation of heart failure patients increases with increasing infections.32 For these reasons, hospital admissions of heart failure patients can be expected to increase after major natural disasters. After natural disasters, if suitable accommodation environments, proper nutrition, access to medicines, and hygienic environment are provided, worsening due to heart failure will be prevented.33

Effect of earthquakes on hypertension

Disasters are a serious source of stress for the body. With stress, physiological mechanisms are activated in the body, the sympathetic system and hypothalamic-pituitary-adrenal axis are activated, and the release of catecholamines and cortisol in the blood increases.34 With this mechanism, an increase in blood pressure and an increase in hypertension and related cardiovascular events are expected in individuals under stress.35

In a study conducted during the Hanshin-Awaji earthquake, it was observed that hypertension patients with normally controlled blood pressure had high blood pressure in the 7-14 days after the earthquake, but regressed to the normal limits in the following 4-6 months.36 Nishizawa also stated that blood pressure increase is transient after earthquakes and it mostly return to normal levels after the fourth week.37 The post-earthquake elevation in blood pressure may be permanent in the elderly, those with chronic renal failure and microalbuminuria, metabolic syndrome or obese patients.37-39

In addition to the acute, subacute and chronic stress caused by the earthquake, dietary and salt intake habits may change, alcohol intake may increase, and weight gain may occur, which may cause metabolic disorders in the long term. This may lead to an increase in chronic diseases.2,29,40 A study examining the incidence of post-earthquake hypertension in the long term was conducted by Ohira et al.41 after the Great East Japan earthquake. When the individuals who were evacuated after the earthquake in Fukushima were examined in the 2-year follow-up, it was observed that the development of hypertension increased especially in males. Also Kobari et al.40, in their 7-year follow-up study after the Great East Japan earthquake, stated that the development of hypertension increased in earthquake victims. It has been determined that the reasons for this increase are the development of obesity in the affected individuals, the increase in alcohol consumption and evacuation from their settlements.

Effect of earthquakes on sudden cardiac death

The increase in cardiovascular-related deaths after major earthquakes has been discussed in previous studies.23,25,42 When the 1994 Northridge earthquake was examined, it was determined that the incidence of sudden cardiac death in earthquake patients increased by 5 times on the day of the earthquake compared to previous years.42 In the 1981 Athens earthquake, it was determined that sudden cardiac deaths increased in the first days after the earthquake.43 In a similar study by Klooner et al.44, it was determined that cardiac deaths increased within 14 days after the earthquake, and then decreased. During the Hanshin-Awaji earthquake, the incidence of cardiac death remained high for 4 months and then returned to normal limits.45 In a study conducted in a single center in Iwake Prefecture during the Great East Japan earthquake, although an increase was found in the number of out-of-hospital cardiac arrests in the 3-week period after the earthquake, the difference was not statistically significant.20

It has been suggested that the mechanism underlying the increase in cardiac deaths after physical or emotional stress is the increased release of catecholamine and hypercoagulability factors after stress, which in turn may lead to coronary artery thrombosis by causing plaque rupture.42,46-48 Emotional stress-induced myocardial ischemia and triggering of severe arrhythmias are likely to be the underlying mechanisms.42

Conclusion

Major natural events such as earthquakes cause serious loss of life and property, especially if the construction is not suitable for earthquakes. The survivors are exposed to life-threatening health problems, both secondary to trauma and organ damage. Survivors of the earthquake without physical injury are exposed to acute and chronic stress due to the earthquake, loss of life of their relatives, and having to leave their settlements. Studies have shown that there is an increase in cardiovascular diseases in the short and long term in individuals who have experienced earthquakes. The reasons for this increase may be the activation of the autonomic nervous system due to physical and mental stress, increase in blood pressure, inability to reach the medications they take routinely due to chronic diseases, and increase in salt intake as a result eating preserved food. In the light of this information, minimizing the post-earthquake stress and taking the necessary precautions for the continuation of appropriate health services, especially in individuals with underlying cardiovascular disease, will minimize the damage due to cardiovascular diseases.

Conflict of interest statement

The authors declare that they have no financial conflict of interest with regard to the content of this report.

Funding source

The authors received no financial support for the research, authorship, and/or publication of this article.

Author Contributions

All authors contributed equally to the article. All authors read and approved the final manuscript.

References

  1. Koçan N, Sürün S. 1. Derece Deprem Kuşağında Yer Alan Balıkesir-Burhaniye Kenti İçin Deprem Parkı Önerisi. Nevşehir Bilim ve Teknol Derg. 2020;9(1):14–31.
  2. https://doi.org/10.17100/nevbiltek.681336
  3. Takahashi S, Nakamura M, Yonekura Y, et al. Association between relocation and changes in cardiometabolic risk factors: a longitudinal study in tsunami survivors of the 2011 Great East Japan Earthquake. BMJ Open. 2016;6(5):e011291.
  4. https://doi.org/10.1136/bmjopen-2016-011291
  5. Kario K, McEwen BS, Pickering TG. Disasters and the heart: a review of the effects of earthquake-induced stress on cardiovascular disease. Hypertens Res Off J Jpn Soc Hypertens. 2003;26(5):355–67. https://doi.org/10.1291/hypres.26.355
  6. McEwen BS, Stellar E. Stress and the individual. Mechanisms leading to disease. Arch Intern Med. 1993;153(18):2093–101.
  7. McEwen BS. Protective and damaging effects of stress mediators. N Engl J Med. 1998;338(3):171–9.
  8. https://doi.org/10.1056/NEJM199801153380307
  9. Rozanski A, Blumenthal JA, Kaplan J. Impact of psychological factors on the pathogenesis of cardiovascular disease and implications for therapy. Circulation. 1999;99(16):2192–217.
  10. https://doi.org/10.1161/01.cir.99.16.2192
  11. James GD, Schlussel YR, Pickering TG. The association between daily blood pressure and catecholamine variability in normotensive working women. Psychosom Med. 1993;55(1):55–60. https://doi.org/10.1097/00006842-199301000-00010
  12. Pickering TG, Devereux RB, James GD, et al. Environmental influences on blood pressure and the role of job strain. J Hypertens Suppl Off J Int Soc Hypertens. 1996;14(5):S179-185.
  13. Schnall PL, Schwartz JE, Landsbergis PA, et al. A longitudinal study of job strain and ambulatory blood pressure: results from a three-year follow-up. Psychosom Med. 1998;60(6):697–706.
  14. https://doi.org/10.1097/00006842-199811000-00007
  15. Pickering T. Cardiovascular pathways: socioeconomic status and stress effects on hypertension and cardiovascular function. Ann N Y Acad Sci. 1999;896:262–77.
  16. https://doi.org/10.1111/j.1749-6632.1999.tb08121.x
  17. Yildirim ÖT, Turgay A, Tunay DL. COVID-19 Pandemisi ve Kardiyovasküler Etkileri. Çukurova Anestezi ve Cerrahi Bilim Derg. 2020;3(3):128–33.
  18. https://doi.org/10.36516/jocass.2020.48
  19. Yıldırım ÖT, Yıldırır A, Sade LE, et al. Is there a relationship between resistin levels and left ventricular end-diastolic pressure? Anatol J Cardiol. 2018 Apr;19(4):267–72.
  20. https://doi.org/10.14744/AnatolJCardiol.2018.66181
  21. Bazoukis G, Tse G, Naka KK, et al. Impact of major earthquakes on the incidence of acute coronary syndromes - A systematic review of the literature. Hell J Cardiol HJC Hell Kardiologike Epitheorese. 2018;59(5):262–7.
  22. https://doi.org/10.1016/j.hjc.2018.05.005
  23. Turgay Yildirim O, Gonullu E, Aydin F, et al. Nocturnal blood pressure dipping is similar in rheumatoid arthritis patients as compared to a normal population. Z Rheumatol. 2019;78(2):190–4.
  24. https://doi.org/10.1007/s00393-018-0451-4
  25. Swerdel JN, Janevic TM, Cosgrove NM, et al. Myocardial Infarction Data Acquisition System (MIDAS 24) Study Group. The effect of Hurricane Sandy on cardiovascular events in New Jersey. J Am Heart Assoc. 2014;3(6):e001354.
  26. https://doi.org/10.1161/JAHA.114.001354
  27. Itoh T, Nakajima S, Tanaka F, et al. Impact of the Japan earthquake disaster with massive Tsunami on emergency coronary intervention and in-hospital mortality in patients with acute ST-elevation myocardial infarction. Eur Heart J Acute Cardiovasc Care. 2014;3(3):195–203.
  28. https://doi.org/10.1177/2048872614538388
  29. Yamaki T, Nakazato K, Kijima M, et al. Impact of the Great East Japan Earthquake on acute myocardial infarction in Fukushima prefecture. Disaster Med Public Health Prep. 2014;8(3):212–9. https://doi.org/10.1017/dmp.2014.37
  30. Aoki T, Fukumoto Y, Yasuda S, et al. The Great East Japan Earthquake Disaster and cardiovascular diseases. Eur Heart J. 2012;33(22):2796–803. https://doi.org/10.1093/eurheartj/ehs288
  31. Tanaka F, Makita S, Ito T, et al. Relationship between the seismic scale of the 2011 northeast Japan earthquake and the incidence of acute myocardial infarction: A population-based study. Am Heart J. 2015;169(6):861–9.
  32. https://doi.org/10.1016/j.ahj.2015.02.007
  33. Nozaki E, Nakamura A, Abe A, et al. Occurrence of cardiovascular events after the 2011 Great East Japan Earthquake and tsunami disaster. Int Heart J. 2013;54(5):247–53.
  34. https://doi.org/10.1536/ihj.54.247
  35. Nakamura M, Tanaka K, Tanaka F, et al. Long-Term Effects of the 2011 Japan Earthquake and Tsunami on Incidence of Fatal and Nonfatal Myocardial Infarction. Am J Cardiol. 2017;120(3):352–8. https://doi.org/10.1016/j.amjcard.2017.05.002
  36. Suzuki S, Sakamoto S, Miki T, et al. Hanshin-Awaji earthquake and acute myocardial infarction. Lancet Lond Engl. 1995;345(8955):981.
  37. Trichopoulos D, Katsouyanni K, Zavitsanos X, et al. Psychological stress and fatal heart attack: the Athens (1981) earthquake natural experiment. Lancet Lond Engl. 1983;1(8322):441–4.
  38. https://doi.org/10.1016/s0140-6736(83)91439-3
  39. Tsuchida M, Kawashiri MA, Teramoto R, et al. Impact of severe earthquake on the occurrence of acute coronary syndrome and stroke in a rural area of Japan. Circ J Off J Jpn Circ Soc. 2009;73(7):1243–7.
  40. https://doi.org/10.1253/circj.cj-08-0812
  41. Dobson AJ, Alexander HM, Malcolm JA, et al. Heart attacks and the Newcastle earthquake. Med J Aust. 1991;155(11–12):757–61. https://doi.org/10.5694/j.1326-5377.1991.tb94029.x.
  42. Brown DL. Disparate effects of the 1989 Loma Prieta and 1994 Northridge earthquakes on hospital admissions for acute myocardial infarction: importance of superimposition of triggers. Am Heart J. 1999;137(5):830–6.
  43. https://doi.org/10.1016/s0002-8703(99)70406-0
  44. Chan C, Elliott J, Troughton R, et al. Acute Myocardial Infarction and Stress Cardiomyopathy following the Christchurch Earthquakes. PLoS ONE. 2013;8(7):e68504.
  45. https://doi.org/10.1371/journal.pone.0068504
  46. Lin LY, Wu CC, Liu YB, et al. Derangement of heart rate variability during a catastrophic earthquake: a possible mechanism for increased heart attacks. Pacing Clin Electrophysiol PACE. 2001;24(11):1596–601.
  47. https://doi.org/10.1046/j.1460-9592.2001.01596.x
  48. Tsubokura M, Takita M, Matsumura T, et al. Changes in metabolic profiles after the Great East Japan Earthquake: a retrospective observational study. BMC Public Health. 2013;13:267.
  49. https://doi.org/10.1186/1471-2458-13-267
  50. Grippo AJ, Johnson AK. Stress, depression and cardiovascular dysregulation: a review of neurobiological mechanisms and the integration of research from preclinical disease models. Stress Amst Neth. 2009;12(1):1–21.
  51. https://doi.org/10.1080/10253890802046281
  52. Azuma T, Seki N, Tanabe N, et al. Prolonged effects of participation in disaster relief operations after the Mid-Niigata earthquake on increased cardiovascular risk among local governmental staff. J Hypertens. 2010;28(4):695–702.
  53. https://doi.org/10.1097/HJH.0b013e328336ed70
  54. Takahashi H, Fujimura S, Ubukata S, et al. Pneumonia after Earthquake, Japan, 2011. Emerg Infect Dis. 2012;18(11):1909–11. https://doi.org/10.3201/eid1811.111660
  55. Yamauchi H, Yoshihisa A, Iwaya S, et al. Clinical features of patients with decompensated heart failure after the Great East Japan Earthquake. Am J Cardiol. 2013;112(1):94–9.
  56. https://doi.org/10.1016/j.amjcard.2013.02.057
  57. Godoy LD, Rossignoli MT, Delfino-Pereira P, et al. A Comprehensive Overview on Stress Neurobiology: Basic Concepts and Clinical Implications. Front Behav Neurosci. 2018;12:127.
  58. https://doi.org/10.3389/fnbeh.2018.00127
  59. Fath AR, Aglan A, Platt J, et al. Chronological Impact of Earthquakes on Blood Pressure: A Literature Review and Retrospective Study of Hypertension in Haiti Before and After the 2010 Earthquake. Front Public Health. 2020;8:600157.
  60. https://doi.org/10.3389/fpubh.2020.600157
  61. Kario K, Matsuo T, Kobayashi H, et al. Earthquake-induced potentiation of acute risk factors in hypertensive elderly patients: possible triggering of cardiovascular events after a major earthquake. J Am Coll Cardiol. 1997;29(5):926–33.
  62. https://doi.org/10.1016/s0735-1097(97)00002-8
  63. Nishizawa M, Hoshide S, Shimpo M, et al. Disaster hypertension: experience from the great East Japan earthquake of 2011. Curr Hypertens Rep. 2012;14(5):375–81.
  64. https://doi.org/10.1007/s11906-012-0298-z
  65. Kario K, Matsuo T, Ishida T, et al. “White coat” hypertension and the Hanshin-Awaji earthquake. Lancet Lond Engl. 1995;345(8961):1365.
  66. https://doi.org/10.1016/s0140-6736(95)92561-9
  67. Kario K, Matsuo T, Shimada K, et al. Factors associated with the occurrence and magnitude of earthquake-induced increases in blood pressure. Am J Med. 2001;111(5):379–84.
  68. https://doi.org/10.1016/s0002-9343(01)00832-4
  69. Kobari E, Tanaka K, Nagao M, et al. Impact of lifestyle and psychosocial factors on the onset of hypertension after the Great East Japan earthquake: a 7-year follow-up of the Fukushima Health Management Survey. Hypertens Res Off J Jpn Soc Hypertens. 2022;45(10):1609–21.
  70. https://doi.org/10.1038/s41440-022-00968-3
  71. Ohira T, Hosoya M, Yasumura S, et al. Evacuation and Risk of Hypertension After the Great East Japan Earthquake: The Fukushima Health Management Survey. Hypertens Dallas Tex 1979. 2016;68(3):558–64.
  72. https://doi.org/10.1161/hypertensionaha.116.07499
  73. Leor J, Poole WK, Kloner RA. Sudden cardiac death triggered by an earthquake. N Engl J Med. 1996;334(7):413–9.
  74. https://doi.org/10.1056/NEJM199602153340701
  75. Katsouyanni K, Kogevinas M, Trichopoulos D. Earthquake-related stress and cardiac mortality. Int J Epidemiol. 1986;15(3):326–30.
  76. https://doi.org/10.1093/ije/15.3.326
  77. Kloner RA, Leor J, Poole WK, et al. Population-based analysis of the effect of the Northridge Earthquake on cardiac death in Los Angeles County, California. J Am Coll Cardiol. 1997;30(5):1174–80.
  78. https://doi.org/10.1016/s0735-1097(97)00281-7
  79. Kario K, Ohashi T. Increased coronary heart disease mortality after the Hanshin-Awaji earthquake among the older community on Awaji Island. Tsuna Medical Association. J Am Geriatr Soc. 1997;45(5):610–3.
  80. https://doi.org/10.1111/j.1532-5415.1997.tb03096.x
  81. Muller JE, Tofler GH. Triggering and hourly variation of onset of arterial thrombosis. Ann Epidemiol. 1992;2(4):393–405.
  82. https://doi.org/10.1016/1047-2797(92)90088-8
  83. Muller JE, Abela GS, Nesto RW, et al. Triggers, acute risk factors and vulnerable plaques: the lexicon of a new frontier. J Am Coll Cardiol. 1994;23(3):809–13.
  84. https://doi.org/10.1016/0735-1097(94)90772-2
  85. Willich SN, Maclure M, Mittleman M, et al. Sudden cardiac death. Support for a role of triggering in causation. Circulation. 1993;87(5):1442–50.
  86. https://doi.org/10.1161/01.cir.87.5.1442

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