A prospective study of the incidence of myocarditis/pericarditis and new onset cardiac symptoms following smallpox and influenza vaccination

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Engler, Renata J M ^a,b   Nelson, Michael R ^a,b   Collins, Limone C ^a   Spooner, Christina ^a   Hemann, Brian A ^a,c   Gibbs, Barnett T ^a,c   Atwood, J Edwin ^a,c   Howard, Robin S ^a   Chang, Audrey S ^a   Cruser, Daniel L ^d   Gates, Daniel G ^e   Vernalis, Marina N ^a   Lengkeek, Marguerite S ^f   McClenathan, Bruce M ^g   Jaffe, Allan S ^h   Cooper, Leslie T ^h   Black, Steve ⁱ   Carlson, Christopher ^j   Wilson, Christopher ^k,n   Davis, Robert L ^l,m  

^a WALTER REED ARMY MEDICAL CENTER   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^c Uniformed Services University of the Health Sciences and the Walter Reed National Military Medical Center   (United States)

^d Vassar Brothers Medical Center   (United States)

^e FORT BELVOIR COMMUNITY HOSPITAL   (United States)

^f Allergy and Asthma Care Centers   (United States)

^g WOMACK ARMY MEDICAL CENTER   (United States)

^h MAYO CLINIC   (United States)

ⁱ CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^j Fred Hutchinson Cancer Research Center   (United States)

^k UNIVERSITY OF WASHINGTON   (United States)

^l UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^m OAK RIDGE NATIONAL LABORATORY   (United States)

ⁿ BILL AND MELINDA GATES FOUNDATION   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

INFLUENZA VACCINE; SMALLPOX VACCINE; TROPONIN T; INACTIVATED VACCINE;

ADULT; ARTICLE; CAUCASIAN; CLINICAL FEATURE; COHORT ANALYSIS; DISEASE SEVERITY; DISEASE SURVEILLANCE; DYSPNEA; FEMALE; HEART DISEASE; HEART PALPITATION; HUMAN; INCIDENCE; INFLUENZA; INFLUENZA VACCINATION; MAJOR CLINICAL STUDY; MALE; MULTICENTER STUDY; MYOCARDITIS; NEW ONSET CARDIAC SYMPTOM; PATIENT ASSESSMENT; PERICARDITIS; POPULATION RESEARCH; PROSPECTIVE STUDY; PROTEIN DETERMINATION; REFERENCE VALUE; SMALLPOX; SYMPTOM; THORAX PAIN; ADVERSE EFFECTS; CLINICAL TRIAL; DEMOGRAPHY; IMMUNOLOGY; METABOLISM; TREATMENT OUTCOME; UNITED STATES; VACCINATION;

TIPULA IRIDESCENT VIRUS; VARIOLA VIRUS;

ADULT; COHORT STUDIES; DEMOGRAPHY; FEMALE; HUMANS; INCIDENCE; INFLUENZA VACCINES; MALE; MYOCARDITIS; PERICARDITIS; PROSPECTIVE STUDIES; SMALLPOX VACCINE; TREATMENT OUTCOME; TROPONIN T; UNITED STATES; VACCINATION; VACCINES, INACTIVATED;

EID: 84925625364     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118283     Document Type: Article

References (53)

1. Smallpox Vaccine Doses Data obtained from the Armed Forces Health Surveillance Center (AFHSC: www.afhsc.mil/home): Defense Medical Surveillance System (DMSS)/Defense Enrollment Eligibility Registry System (DEERS) Immunization Registry: 14 March 2012.
2. Nalca A, Zumbrun EE. ACAM2000: the new smallpox vaccine for United States Strategic National Stockpile. Drug Des Devel Ther. 2010 May 25; 4:71-9. PMID: 20531961
3. Arness MK, Eckart RE, Love SS, Atwood JE, Wells TS, Engler RJ, et al. Myo/pericarditis following smallpox vaccination. Am J Epidemiol. 2004 Apr; 160(7):642-51. PMID: 15383408
4. Eckart RE, Love SS, Atwood JE, Arness MK, Cassimatis DC, Campbell CL, et al. and the Department of Defense Smallpox Vaccination Clinical Evaluation Team. Incidence and follow-up of inflammatory cardiac complications after smallpox vaccination. J Am Coll Cardiol. 2004 Jul; 44(1):201-5. PMID: 15234435
5. Smallpox Vaccine. Vaccines and Related Biological Products Advisory Committee (VRBPAC) Briefing Document, 18 April 2007. Available: www.fda.gov/ohrms/dockets/ac/07/briefing/2007-4292b2-02.pdf. Accessed 2012 Oct 4.
6. Varricchio F, Iskander J, Destefano F, Ball R, Pless R, Braun MM, et al. Understanding vaccine safety information from the Vaccine Adverse Event Reporting System. Pediatr Infect Dis J. 2004 Apr; 23 (4):287-94. PMID: 15071280
7. McMahon AW, Zinderman C, Ball R, Gupta G, Braun MM. Comparison of military and civilian reporting rates for smallpox vaccine adverse events. Pharmacoepidemiol Drug Saf. 2007; 16(6):597-604. PMID: 17154344
8. Memorandum for Secretaries of the Military Departments, Chairman of the Joint Chiefs of Staff, Under Secretaries of Defense, General Counsel of the Department of Defense, Directors of Defense Agencies, Commandant of the U.S. Coast Guard: Subject: Update to Clinical Policy for the Department of Defense Smallpox Vaccination Program; dated April 1, 2008, HA Policy 08- 004. Available: www. vaccines.mil/documents/1182SPX-Update-Clinical-Policy.pdf. Accessed 2013 Jul 30.
9. Rautaharju PM, Surawicz B, Gettes LS, Bailey JJ, Childers R, Deal BJ, et al. American Heart Association Electrocardiography and Arrhythmias Committee, Council on Clinical Cardiology; American College of Cardiology Foundation; Heart Rhythm Society. AHA/ACCF/HRS Recommendations for the Standardization and Interpretation of the Electrocardiogram, Part IV: The ST Segment, T and U Waves and the QT Interval: a scientific statement from the American Heart Association Electrocardiography and Arrhythmias Committee, Council on Clinical Cardiology; the American College of Cardiology Foundation; and the Heart Rhythm Society. Endorsed by the International Society for Computerized Electrocardiology. J Am Coll Cardiol 2009 Mar 17; 53(11):982-91. doi: 10.1016/j.jacc.2008.12.014 PMID: 19281931
10. th percentile reference limits for cardiac troponin and creatine kinase MB mass for use with European Society of Cardiology/American College of Cardiology consensus recommendations. Clin Chem 2003 Aug; 49(8):1331-6. PMID: 12881449
11. Zarich SW, Bradley K, Mayall ID, Bernstein LH. Minor elevations in troponin T values enhance risk assessment in emergency department patients with suspected myocardial ischemia: analysis of novel troponin T cut-off values. Clin Chim Acta. 2004 May; 343(1-2):223-9. PMID: 15115702
12. Wallace TW, Abdullah SM, Drazner MH, Das SR, Khera A, McGuire DK, et al. Prevalence and determinants of troponin T elevation in the general population. Circulation 2006 Apr 25, 113(16):1958-1965. PMID: 16618821
13. Thygesen K, Mair J, Katus H, Plebani M, Venge P, Collinson P, et al.; Study Group on Biomarkers in Cardiology of the ESC Working Group on Acute Cardiac Care. Recommendations for the use of cardiac troponin measurement in acute cardiac care. Eur Heart J. 2010 Sep; 31(18):2197-204. doi: 10.1093/ eurheartj/ehq251 PMID: 20685679
14. de Lemos JA, Drazner MH, Omland T, Ayers CR, Khera A, Rohtagi A, et al. Association of troponin T detected with a highly sensitive assay and cardiac structure and mortality risk in the general population. JAMA 2010 Dec 8; 304(22):2503-12. doi: 10.1001/jama.2010.1768 PMID: 21139111
15. de Lemos JA. Increasingly sensitive assays for cardiac troponins: a review. JAMA 2013 Jun 5; 309 (21):2262-9. doi: 10.1001/jama.2013.5809 PMID: 23736735
16. Morgan J, Roper MH, Sperling L, Schieber RA, Heffelfinger JD, Casey CG, et al. Myocarditis, pericarditis, and dilated cardiomyopathy after smallpox vaccination among civilians in the United States, Janu-ary-October 2003. Clin Infect Dis. 2008 Mar 15; 46 Suppl 3:S242-50. doi: 10.1086/524747 PMID: 18284365
17. Cohen JI, Hohman P, Fulton R, Turk SP, Quin J, Thatcher K, et al. Kinetics of serum cytokines after primary or repeat vaccination with the smallpox vaccine. J Infect Dis. 2010 Apr 15;15; 201(8):1183-91. doi: 10.1086/651453 PMID: 20214479
18. Haim M, Gdalevich M, Mimouni D, Ashkenazi I, Shemer J. Adverse reactions to smallpox vaccine: the Israel Defense Force experience, 1991 to 1996. A comparison with previous surveys. Mil Med. 2000 Apr; 165(4):287-9. PMID: 10803002
19. Lane JM, Goldstein J. Evaluation of 21st-Century Risks of Smallpox Vaccination and Policy Options. Ann Intern Med 2003 Mar 18; 138(6):488-493. PMID: 12639083
20. Ahlborg B, Linroth K, Nordgren B. ECG changes without subjective symptoms after smallpox vaccination of military personnel. Acta Med Scand Suppl. 1966; 464:127-134. PMID: 5229008
21. Karjalainen J, Heikkilä J, Nieminen MS, Jalanko H, Kleemola M, Lapinleimu, et al. Etiology of mild acute infectious myocarditis. Relation to clinical features. Acta Med Scand. 1983; 213(1):65-73. PMID: 6829323
22. Friman G. The incidence and epidemiology of myocarditis. Eur Heart J 1999 Aug; 20(15):1063-66. PMID: 10413634
23. Baggs J, Chen RT, Damon IK, Rotz L, Allen C, Fullerton KE, et al. Safety profile of smallpox vaccine: insights from the laboratory worker smallpox vaccination program. Clin Infect Dis. 2005 Apr 15; 40 (8):1133-40. PMID: 15791513
24. Sniadack MM, Neff LJ, Swerdlow DL, Schieber RA, McCauley MM, Mootrey GT. Follow-up of Cardiovascular Adverse Events after Smallpox Vaccination among civilians in the United States, 2003. Clin Infect Dis 2008 Mar; 46: Suppl 3:S251-7. doi: 10.1086/524741 PMID: 18284366
25. Reif DM, McKinney BA, Motsinger AA, Chanock SJ, Edwards KM, Rock MT, et al. Genetic basis for adverse events after smallpox vaccination. J Infect Dis. 2008 Jul 1; 198(1):16-22. doi: 10.1086/588670 PMID: 18454680
26. Reif DM, Motsinger-Reif AA, McKinney BA, Rock MT, Crowe JE Jr, Moore JH. Integrated analysis of genetic and proteomic data identifies biomarkers associated with adverse events following smallpox vaccination. Genes Immun. 2009 Mar; 10(2):112-9. doi: 10.1038/gene.2008.80 PMID: 18923431
27. Sagar S, Liu PP, Cooper LT. Myocarditis. Lancet 2012 Feb 25; 379:738-747. doi: 10.1016/S0140-6736(11)60648-X PMID: 22185868
28. Soongswang J, Durongpisitkul K, Nana A, Laohaprasittiporn D, Kangkagate C, Punlee K, et al. Cardiac troponin T: a marker in the diagnosis of acute myocarditis in children. Pediatr Cardiol. 2005 Jan-Feb; 26:45-9. PMID: 15793653
29. Lauer B, Niederau C, Kuhl U, Schannwell M, Pauschinger M, Strauer BE, et al. Cardiac troponin T in patients with clinically suspected myocarditis. J Am Coll Cardiol 1997 Nov 1; 30(5):1354-9. PMID: 9350939
30. Sano J, Chaitman BR, Swindle J, Frey SE. Electrocardiography screening for cardiotoxicity after modified Vaccinia Ankara vaccination. Am J Med. 2009 Jan 1; 122(1):79-84. doi: 10.1016/j.amjmed.2008. 07.025 PMID: 19114175
31. Elizaga ML, Vasan S, Marovich MA, Sato AH, Lawrence DN, Chaitman BR, et al.; MVA Cardiac Safety Working Group. Prospective surveillance for cardiac adverse events in healthy adults receiving modified vaccinia Ankara vaccines: a systematic review. PLoS One. 2013;8(1):e54407. Available: http:// www.ncbi.nlm.nih.gov/pmc/articles/PMC3547923/pdf/pone.0054407.pdf. Accessed 2013Aug 30.
32. Cramer GE, Brouwer MA, Vader HL, de Boer MJ, Pop GA, Pop VJ, et al. Highly sensitive cardiac troponin T and long-term mortality in a population of community-derived perimenopausal women: nested case-control study. Heart. 2013 Apr; 99(8):528-33. doi: 10.1136/heartjnl-2012-302829 PMID: 23315610
33. Thygesen K, Alpert JS, Jaffe AS, Simoons ML, Chaitman BR, White HD. Joint ESC/ACCF/AHA/WHF Task Force for the Universal Definition of Myocardial Infarction. Third universal definition of myocardial infarction. Circulation. 2012;126:2020-2035. Available: http://www.escardio.org/guidelines-surveys/ esc-guidelines/GuidelinesDocuments/guidelines-universal-MI-slides.pdf. Accessed 2013 Oct 1.
34. Sabatine MS, Morrow DA, de Lemos JA, Jarolim P, Braunwald E. Detection of acute changes in circulating troponin in the setting of transient stress test-induced myocardial ischaemia using an ultrasensitive assay: results from TIMI 35. Eur Heart J. 2009 Jan; 30(2):162-9. doi: 10.1093/eurheartj/ehn504 PMID: 18997177
35. Babuin L, Vasile VC, Rio Perez JA, Alegria JR, Chai HS, Afessa B, et al. Elevated cardiac troponin is an independent risk factor for short- and long-term mortality in medical intensive care unit patients. Crit Care Med 2008 Mar; 36(3):759-765. doi: 10.1097/CCM.0B013E318164E2E4 PMID: 18209672
36. Oluleye OW, Folsom AR, Nambi V, Lutsey PL, Ballantyne CM; ARIC Study Investigators. Troponin T, B-type natriuretic peptide, C-reactive protein, and cause-specific mortality. Ann Epidemiol. 2013 Feb; 23(2):66-73. doi: 10.1016/j.annepidem.2012.11.004 PMID: 23228375
37. Mascaro-Blanco A, Alvarez K, Yu X, Lindenfeld J, Olansky L, Lyons T, et al. Consequences of unlocking the cardiac myosin molecule in human myocarditis and cardiomyopathies. Autoimmunity 2008 Sep; 41(6):442-53. doi: 10.1080/08916930802031579 PMID: 18781470
38. Rose NR. Critical cytokine pathways to cardiac inflammation. J Interferon Cytokine Res. 2011 Oct; 31 (10):705-10. doi: 10.1089/jir.2011.0057 PMID: 21861699
39. Libby P, Lichtman AH, Hansson GK. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity. 2013 Jun 27; 38(6):1092-104. doi: 10.1016/j.immuni.2013.06.009 PMID: 23809160
40. Kao CD, Chen JT, Lin KP, Shan DE, Wu ZA, Liao KK. Guillain-Barré syndrome coexisting with pericarditis or nephrotic syndrome after influenza vaccination. Clin Neurol Neurosurg. 2004 Mar; 106(2):136-8. PMID: 15003306
41. de Meester A, Luwaert R, Chaudron JM. Symptomatic pericarditis after influenza vaccination: report of two cases. Chest. 2000 Jun; 117(6):1803-5. PMID: 10858422
42. Eckart RE, Shry EA, Atwood JE, Brundage JF, Lay JC, Bateson TF, et al. Smallpox vaccination and ischemic coronary events in healthy adults. Vaccine 2007 Dec 5; 25(50):8359-64. PMID: 17981378
43. Jacobson IG, Smith TC, Smith B, Wells TS, Reed RJ, Ryan MA. US military service members vaccinated against smallpox in 2003 and 2004 experience a slightly higher risk of hospitalization post-vaccination. Vaccine. 2008 Jul 29; 26(32):4048-56. doi: 10.1016/j.vaccine.2008.05.044 PMID: 18586364
44. Shave R, Baggish A, George K, Wood M, Scharhag J, Whyte G, et al. Exercise-induced cardiac troponin elevation: evidence, mechanisms, and implications. J Am Coll Cardiol. 2010 Jul 13; 56(3):169-76. doi: 10.1016/j.jacc.2010.03.037 PMID: 20620736
45. Harper RW. Exercise-induced troponin elevation: not necessarily a benign phenomenon. J Am CollCardio 2010 Dec 14; 56(25):2145.
46. Regwan S, Hulten EA, Martinho S, Slim J, Villines TC, Mitchell J, et al. Marathon running as a cause of troponin elevation: a systematic review and meta-analysis. J Interv Cardiol. 2010 Oct; 23(5):443-50. doi: 10.1111/j.1540-8183.2010.00575.x PMID: 20663014
47. Baker P, Davies SL, Larkin J, Moult D, Benton S, Roberts A, et al. Changes to the cardiac biomarkers of non-elite athletes completing the 2009 London Marathon. Emerg Med J. 2014 May; 31(5):374-9. doi: 10.1136/emermed-2012-201465 PMID: 23513235
48. Tian Y, Nie J, Huang C, George KP. The kinetics of highly sensitive cardiac troponin T release after prolonged treadmill exercise in adolescent and adult athletes. J Appl Physiol. 2012 Aug; 113(3):418-25. doi: 10.1152/japplphysiol.00247.2012 PMID: 22653984
49. deFilippi CR, de Lemos JA, Tkaczuk AT, Christenson RH, Carnethon MR, Siscovick DS, et al. Physical activity, change in biomarkers of myocardial stress and injury, and subsequent heart failure risk in older adults. J Am Coll Cardiol. 2012 Dec 18; 60(24):2539-47. doi: 10.1016/j.jacc.2012.08.1006 PMID: 23158528
50. Falkensammer J, Gasteiger S, Stojakovic T, Stühlinger M, Scharnagl H, Frech A, et al. Elevated baseline hs-cTnT levels predict exercise-induced myocardial ischemia in patients with peripheral arterial disease. Clin Chim Acta. 2012 Dec 18; 413(19-20):1678-82.
51. Pervanidou P, Akalestos A, Bastaki D, Apostolakou F, Papassotiriou I, Chrousos G. Increased circulating High-Sensitivity Troponin T concentrations in children and adolescents with obesity and the metabolic syndrome: a marker for early cardiac damage? Metabolism. 2013 Apr; 62(4):527-31. doi: 10. 1016/j.metabol.2012.09.012 PMID: 23114876
52. Elizaga ML, Vasan S, Marovich MA, Sato AH, Lawrence DN, Chaitman BR, et al.; MVA Cardiac Safety Working Group. Prospective surveillance for cardiac adverse events in healthy adults receiving modified vaccinia Ankara vaccines: a systematic review. PLoS One. 2013; 8(1):e54407. doi: 10.1371/ journal.pone.0054407 PMID: 23349878
53. Montgomery JR, Engler R, Allan-Martinez F, Morse A, Duran L. Case report: Chest pain in service members following smallpox vaccination. MSMR. 2012 Mar; 19(3):6-7. PMID: 22452714