Echocardiographic and Electrocardiographic Findings in Patients with Ankylosing Spondylitis without Cardiovascular Risk Factors
,
Abstract
Background: Ankylosing spondylitis (AS) is a chronic inflammatory condition associated with more cardiac manifestations than those in the normal population. In this study, we sought to determine the prevalence of cardiac involvement in patients suffering from AS without cardiovascular risk factors.
Methods: The present case-control study, conducted in 2 university hospitals in Tehran from January 2016 to December 2017, recruited 67 patients with AS and 40 age- and sex-matched healthy controls. The diagnosis of AS was based on the classification criteria of the Assessment of SpondyloArthritis International Society. All the participants were examined using transthoracic echocardiography and a standard 12-lead ECG. Baseline characteristics, echocardiographic findings, and ECG features were compared between the AS and control groups using univariate analyses.
Results: The median age was 33.5 (IQR25-75%: 20.5–59) years in the AS group and 35 (IQR25-75%: 26–59) years in the control group (P=0.301). The number of patients with left ventricular systolic and diastolic dysfunction was significantly higher in the patients with AS than in the controls (7.5% vs. 20.9%; P=0.067, and 22.9% vs. 5.0%; P=0.026, respectively). The number of individuals with a left-axis deviation and a left anterior fascicular block was significantly higher in the patients suffering from AS than in the control group. The number of patients with aortic valve involvement was comparable between the groups (P=0.332).
Conclusion: The most common cardiac involvement in our patients with AS was left ventricular dysfunction, followed by rhythm disturbances and aortic valve insufficiency. These findings were independent of age, AS severity, and disease duration. Therefore, the implementation of cardiovascular screening can be recommended for patients with AS.
1. Dean LE, Jones GT, MacDonald AG, Downham C, Sturrock RD, Macfarlane GJ. Global prevalence of ankylosing spondylitis. Rheumatology (Oxford) 2014;53:650-657.
2. Momeni M, Taylor N, Tehrani M. Cardiopulmonary manifestations of ankylosing spondylitis. Int J Rheumatol 2011;2011:728471.
3. Amin A, Chitsazan M, Navid H. Left ventricular systolic dysfunction in two patients with ankylosing spondylitis: What is the role of corticosteroids? Eur J Rheumatol 2016;3:179-181.
4. Kang JH, Chen YH, Lin HC. Comorbidity profiles among patients with ankylosing spondylitis: a nationwide population-based study. Ann Rheum Dis 2010;69:1165-1168.
5. Zochling J, Braun J. Mortality in ankylosing spondylitis. Clin Exp Rheumatol 2008;26(5 Suppl 51):S80-84.
6. Ozkan Y. Cardiac involvement in ankylosing spondylitis. J Clin Med Res 2016;8:427-430.
7. Bergfeldt L. HLA-B27-associated cardiac disease. Ann Intern Med 1997;127(8 Pt 1):621-629.
8. Lautermann D, Braun J. Ankylosing spondylitis--cardiac manifestations. Clin Exp Rheumatol 2002;20(6 Suppl 28):S11-15.
9. Roldan CA, Chavez J, Wiest PW, Qualls CR, Crawford MH. Aortic root disease and valve disease associated with ankylosing spondylitis. J Am Coll Cardiol 1998;32:1397-1404.
10. Palazzi C, D' Angelo S, Lubrano E, Olivieri I. Aortic involvement in ankylosing spondylitis. Clin Exp Rheumatol 2008;26(3 Suppl 49):S131-134.
11. Dik VK, Peters MJ, Dijkmans PA, Van der Weijden MA, De Vries MK, Dijkmans BA, Van der Horst-Bruinsma IE, Nurmohamed MT. The relationship between disease-related characteristics and conduction disturbances in ankylosing spondylitis. Scand J Rheumatol 2010;39:38-41.
12. Acar G, Sayarlioglu M, Akcay A, Sokmen A, Sokmen G, Altun B, Nacar AB, Gunduz M, Tuncer C. Assessment of atrial electromechanical coupling characteristics in patients with ankylosing spondylitis. Echocardiography 2009;26:549-557.
13. Kırış A, Karkucak M, Karaman K, Kırış G, Capkın E, Gökmen F, Kutlu M, Çelik Ş, Ayar A. Patients with ankylosing spondylitis have evidence of left ventricular asynchrony. Echocardiography 2012;29:661-667.
14. Yildirir A, Aksoyek S, Calguneri M, Oto A, Kes S. Echocardiographic evidence of cardiac involvement in ankylosing spondylitis. Clin Rheumatol 2002;21:129-134.
15. Ercan S, Goktepe F, Kisacik B, Pehlivan Y, Onat AM, Yavuz F, Alici H, Davutoğlu V. Subclinical cardiovascular target organ damage manifestations of ankylosing spondylitis in young adult patients. Mod Rheumatol 2013;23:1063-1068.
16. Ustun N, Kurt M, Nacar AB, Karateke HP, Guler H, Turhanoglu AD. Left ventricular systolic dysfunction in patients with ankylosing spondylitis without clinically overt cardiovascular disease by speckle tracking echocardiography. Rheumatol Int 2015;35:607-611.
17. Gunes Y, Tuncer M, Guntekin U, Sahin M, Yazmalar L. Effects of ankylosing spondylitis on the heart. Acta Cardiol 2009;64:385-392.
18. Klingberg E, Sveälv BG, Täng MS, Bech-Hanssen O, Forsblad-d'Elia H, Bergfeldt L. Aortic regurgitation is common in ankylosing spondylitis: Time for routine echocardiography evaluation? Am J Med 2015;128:1244-1250.e1.
19. Midtbø H, Gerdts E, Berg IJ, Rollefstad S, Jonsson R, Semb AG. Ankylosing spondylitis is associated with increased prevalence of left ventricular hypertrophy. J Rheumatol 2018;45:1249-1255.
20. Kaya EB, Okutucu S, Aksoy H, Karakulak UN, Tulumen E, Ozdemir O, Inanici F, Aytemir K, Kabakci G, Tokgozoglu L, Ozkutlu H, Oto A. Evaluation of cardiac autonomic functions in patients with ankylosing spondylitis via heart rate recovery and heart rate variability. Clin Res Cardiol 2010;99:803-808.
21. Peters MJ, Visman I, Nielen MM, Van Dillen N, Verheij RA, van der Horst-Bruinsma IE, Dijkmans BA, Nurmohamed MT. Ankylosing spondylitis: a risk factor for myocardial infarction? Ann Rheum Dis 2010;69:579-581.
22. Caliskan M, Erdogan D, Gullu H, Yilmaz S, Gursoy Y, Yildirir A, Yucel E, Muderrisoglu H. Impaired coronary microvascular and left ventricular diastolic functions in patients with ankylosing spondylitis. Atherosclerosis 2008;196:306-312.
23. Toufan M, Pourafkari L, Afrasiabi A, Sohrabi M, Nader ND. Left atrial appendage aneurysm presenting with chronic cough. Neth Heart J 2017;25:526-527.
24. Jamshidi AR, Shahlaee A, Farhadi E, Fallahi S, Nicknam MH, Bidad K, Barghamadi M, Mahmoudi M. Clinical characteristics and medical management of Iranian patients with ankylosing spondylitis. Mod Rheumatol 2014;24:499-504.
25. Soroush M, Mominzadeh M, Ghelich Y, Soroosh S, Pasha MA. Investigation of cardiac complications and their incidence in patients with ankylosing spondylitis. Med Arch 2016;70:35-38.
26. van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 1984;27:361-368.
27. Garrett S, Jenkinson T, Kennedy LG, Whitelock H, Gaisford P, Calin A. A new approach to defining disease status in ankylosing spondylitis: the Bath Ankylosing Spondylitis Disease Activity Index. J Rheumatol 1994;21:2286-2291.
28. Calin A, Garrett S, Whitelock H, Kennedy LG, O'Hea J, Mallorie P, Jenkinson T. A new approach to defining functional ability in ankylosing spondylitis: the development of the Bath Ankylosing Spondylitis Functional Index. J Rheumatol 1994;21:2281-2285.
29. Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelista A. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr 2009;22:107-133.
30. Okan T, Sari I, Akar S, Cece H, Goldeli O, Guneri S, Akkoc N. Ventricular diastolic function of ankylosing spondylitis patients by using conventional pulsed wave Doppler, myocardial performance index and tissue Doppler imaging. Echocardiography 2008;25:47-56.
31. Bengtsson K, Forsblad-d'Elia H, Lie E, Klingberg E, Dehlin M, Exarchou S, Lindström U, Askling J, Jacobsson LTH. Risk of cardiac rhythm disturbances and aortic regurgitation in different spondyloarthritis subtypes in comparison with general population: a register-based study from Sweden. Ann Rheum Dis 2018;77:541-548.
32. Bergfeldt L, Edhag O, Vallin H. Cardiac conduction disturbances, an underestimated manifestation in ankylosing spondylitis. A 25-year follow-up study of 68 patients. Acta Med Scand 1982;212:217-223.
33. Moyssakis I, Gialafos E, Vassiliou VA, Boki K, Votteas V, Sfikakis PP, Tzelepis GE. Myocardial performance and aortic elasticity are impaired in patients with ankylosing spondylitis. Scand J Rheumatol 2009;38:216-221.
34. Biesbroek PS, Heslinga SC, Konings TC, van der Horst-Bruinsma IE, Hofman MBM, van de Ven PM, Kamp O, van Halm VP, Peters MJL, Smulders YM, van Rossum AC, Nurmohamed MT, Nijveldt R. Insights into cardiac involvement in ankylosing spondylitis from cardiovascular magnetic resonance. Heart 2017;103:745-752.
35. Kazmierczak J, Peregud-Pogorzelska M, Biernawska J, Przepiera-Bedzak H, Goracy J, Brzosko I, Plonska E, Brzosko M. Cardiac arrhythmias and conduction disturbances in patients with ankylosing spondylitis. Angiology 2007;58:751-756.
36. Aksoy H, Okutucu S, Sayin BY, Ercan EA, Kaya EB, Ozdemir O, Inanici F, Aytemir K, Oto A. Assessment of cardiac arrhythmias in patients with ankylosing spondylitis by signal-averaged P wave duration and P wave dispersion. Eur Rev Med Pharmacol Sci 2016;20:1123-1129.
37. Mirfeizi Z, Poorzand H, Javanbakht A, Khajedaluee M. Relationship between systemic lupus erythematosus disease activity index scores and subclinical cardiac problems. Iran Red Crescent Med J 2016;18:e38045.
38. Albayrak N, Bayram NA, Erten S, Sari C, Keles T, Durmaz T, Bastug S, Bozkurt E. The effects of undifferentiated spondyloarthropathy on left ventricular systolic and diastolic function. Int J Rheum Dis 2013;16:162-167.
39. Bayram NA, Cicek OF, Erten S, Keles T, Durmaz T, Bilen E, Sarı C, Bozkurt E. Assessment of left ventricular functions in patients with Sjögren's syndrome using tissue Doppler echocardiography. Int J Rheum Dis 2013;16:425-429.
40. Chen Y, Chung HY, Zhao CT, Wong A, Zhen Z, Tsang HH, Lau CS, Tse HF, Yiu KH. Left ventricular myocardial dysfunction and premature atherosclerosis in patients with axial spondyloarthritis. Rheumatology (Oxford) 2015;54:292-301.
41. Sveälv BG, Täng MS, Klingberg E, Forsblad-d'Elia H, Bergfeldt L. Prevalence of diastolic dysfunction in patients with ankylosing spondylitis: a cross-sectional study. Scand J Rheumatol 2015;44:111-117.
42. Heslinga SC, Van Dongen CJ, Konings TC, Peters MJ, Van der Horst-Bruinsma IE, Smulders YM, Nurmohamed MT. Diastolic left ventricular dysfunction in ankylosing spondylitis--a systematic review and meta-analysis. Semin Arthritis Rheum 2014;44:14-19.
2. Momeni M, Taylor N, Tehrani M. Cardiopulmonary manifestations of ankylosing spondylitis. Int J Rheumatol 2011;2011:728471.
3. Amin A, Chitsazan M, Navid H. Left ventricular systolic dysfunction in two patients with ankylosing spondylitis: What is the role of corticosteroids? Eur J Rheumatol 2016;3:179-181.
4. Kang JH, Chen YH, Lin HC. Comorbidity profiles among patients with ankylosing spondylitis: a nationwide population-based study. Ann Rheum Dis 2010;69:1165-1168.
5. Zochling J, Braun J. Mortality in ankylosing spondylitis. Clin Exp Rheumatol 2008;26(5 Suppl 51):S80-84.
6. Ozkan Y. Cardiac involvement in ankylosing spondylitis. J Clin Med Res 2016;8:427-430.
7. Bergfeldt L. HLA-B27-associated cardiac disease. Ann Intern Med 1997;127(8 Pt 1):621-629.
8. Lautermann D, Braun J. Ankylosing spondylitis--cardiac manifestations. Clin Exp Rheumatol 2002;20(6 Suppl 28):S11-15.
9. Roldan CA, Chavez J, Wiest PW, Qualls CR, Crawford MH. Aortic root disease and valve disease associated with ankylosing spondylitis. J Am Coll Cardiol 1998;32:1397-1404.
10. Palazzi C, D' Angelo S, Lubrano E, Olivieri I. Aortic involvement in ankylosing spondylitis. Clin Exp Rheumatol 2008;26(3 Suppl 49):S131-134.
11. Dik VK, Peters MJ, Dijkmans PA, Van der Weijden MA, De Vries MK, Dijkmans BA, Van der Horst-Bruinsma IE, Nurmohamed MT. The relationship between disease-related characteristics and conduction disturbances in ankylosing spondylitis. Scand J Rheumatol 2010;39:38-41.
12. Acar G, Sayarlioglu M, Akcay A, Sokmen A, Sokmen G, Altun B, Nacar AB, Gunduz M, Tuncer C. Assessment of atrial electromechanical coupling characteristics in patients with ankylosing spondylitis. Echocardiography 2009;26:549-557.
13. Kırış A, Karkucak M, Karaman K, Kırış G, Capkın E, Gökmen F, Kutlu M, Çelik Ş, Ayar A. Patients with ankylosing spondylitis have evidence of left ventricular asynchrony. Echocardiography 2012;29:661-667.
14. Yildirir A, Aksoyek S, Calguneri M, Oto A, Kes S. Echocardiographic evidence of cardiac involvement in ankylosing spondylitis. Clin Rheumatol 2002;21:129-134.
15. Ercan S, Goktepe F, Kisacik B, Pehlivan Y, Onat AM, Yavuz F, Alici H, Davutoğlu V. Subclinical cardiovascular target organ damage manifestations of ankylosing spondylitis in young adult patients. Mod Rheumatol 2013;23:1063-1068.
16. Ustun N, Kurt M, Nacar AB, Karateke HP, Guler H, Turhanoglu AD. Left ventricular systolic dysfunction in patients with ankylosing spondylitis without clinically overt cardiovascular disease by speckle tracking echocardiography. Rheumatol Int 2015;35:607-611.
17. Gunes Y, Tuncer M, Guntekin U, Sahin M, Yazmalar L. Effects of ankylosing spondylitis on the heart. Acta Cardiol 2009;64:385-392.
18. Klingberg E, Sveälv BG, Täng MS, Bech-Hanssen O, Forsblad-d'Elia H, Bergfeldt L. Aortic regurgitation is common in ankylosing spondylitis: Time for routine echocardiography evaluation? Am J Med 2015;128:1244-1250.e1.
19. Midtbø H, Gerdts E, Berg IJ, Rollefstad S, Jonsson R, Semb AG. Ankylosing spondylitis is associated with increased prevalence of left ventricular hypertrophy. J Rheumatol 2018;45:1249-1255.
20. Kaya EB, Okutucu S, Aksoy H, Karakulak UN, Tulumen E, Ozdemir O, Inanici F, Aytemir K, Kabakci G, Tokgozoglu L, Ozkutlu H, Oto A. Evaluation of cardiac autonomic functions in patients with ankylosing spondylitis via heart rate recovery and heart rate variability. Clin Res Cardiol 2010;99:803-808.
21. Peters MJ, Visman I, Nielen MM, Van Dillen N, Verheij RA, van der Horst-Bruinsma IE, Dijkmans BA, Nurmohamed MT. Ankylosing spondylitis: a risk factor for myocardial infarction? Ann Rheum Dis 2010;69:579-581.
22. Caliskan M, Erdogan D, Gullu H, Yilmaz S, Gursoy Y, Yildirir A, Yucel E, Muderrisoglu H. Impaired coronary microvascular and left ventricular diastolic functions in patients with ankylosing spondylitis. Atherosclerosis 2008;196:306-312.
23. Toufan M, Pourafkari L, Afrasiabi A, Sohrabi M, Nader ND. Left atrial appendage aneurysm presenting with chronic cough. Neth Heart J 2017;25:526-527.
24. Jamshidi AR, Shahlaee A, Farhadi E, Fallahi S, Nicknam MH, Bidad K, Barghamadi M, Mahmoudi M. Clinical characteristics and medical management of Iranian patients with ankylosing spondylitis. Mod Rheumatol 2014;24:499-504.
25. Soroush M, Mominzadeh M, Ghelich Y, Soroosh S, Pasha MA. Investigation of cardiac complications and their incidence in patients with ankylosing spondylitis. Med Arch 2016;70:35-38.
26. van der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 1984;27:361-368.
27. Garrett S, Jenkinson T, Kennedy LG, Whitelock H, Gaisford P, Calin A. A new approach to defining disease status in ankylosing spondylitis: the Bath Ankylosing Spondylitis Disease Activity Index. J Rheumatol 1994;21:2286-2291.
28. Calin A, Garrett S, Whitelock H, Kennedy LG, O'Hea J, Mallorie P, Jenkinson T. A new approach to defining functional ability in ankylosing spondylitis: the development of the Bath Ankylosing Spondylitis Functional Index. J Rheumatol 1994;21:2281-2285.
29. Nagueh SF, Appleton CP, Gillebert TC, Marino PN, Oh JK, Smiseth OA, Waggoner AD, Flachskampf FA, Pellikka PA, Evangelista A. Recommendations for the evaluation of left ventricular diastolic function by echocardiography. J Am Soc Echocardiogr 2009;22:107-133.
30. Okan T, Sari I, Akar S, Cece H, Goldeli O, Guneri S, Akkoc N. Ventricular diastolic function of ankylosing spondylitis patients by using conventional pulsed wave Doppler, myocardial performance index and tissue Doppler imaging. Echocardiography 2008;25:47-56.
31. Bengtsson K, Forsblad-d'Elia H, Lie E, Klingberg E, Dehlin M, Exarchou S, Lindström U, Askling J, Jacobsson LTH. Risk of cardiac rhythm disturbances and aortic regurgitation in different spondyloarthritis subtypes in comparison with general population: a register-based study from Sweden. Ann Rheum Dis 2018;77:541-548.
32. Bergfeldt L, Edhag O, Vallin H. Cardiac conduction disturbances, an underestimated manifestation in ankylosing spondylitis. A 25-year follow-up study of 68 patients. Acta Med Scand 1982;212:217-223.
33. Moyssakis I, Gialafos E, Vassiliou VA, Boki K, Votteas V, Sfikakis PP, Tzelepis GE. Myocardial performance and aortic elasticity are impaired in patients with ankylosing spondylitis. Scand J Rheumatol 2009;38:216-221.
34. Biesbroek PS, Heslinga SC, Konings TC, van der Horst-Bruinsma IE, Hofman MBM, van de Ven PM, Kamp O, van Halm VP, Peters MJL, Smulders YM, van Rossum AC, Nurmohamed MT, Nijveldt R. Insights into cardiac involvement in ankylosing spondylitis from cardiovascular magnetic resonance. Heart 2017;103:745-752.
35. Kazmierczak J, Peregud-Pogorzelska M, Biernawska J, Przepiera-Bedzak H, Goracy J, Brzosko I, Plonska E, Brzosko M. Cardiac arrhythmias and conduction disturbances in patients with ankylosing spondylitis. Angiology 2007;58:751-756.
36. Aksoy H, Okutucu S, Sayin BY, Ercan EA, Kaya EB, Ozdemir O, Inanici F, Aytemir K, Oto A. Assessment of cardiac arrhythmias in patients with ankylosing spondylitis by signal-averaged P wave duration and P wave dispersion. Eur Rev Med Pharmacol Sci 2016;20:1123-1129.
37. Mirfeizi Z, Poorzand H, Javanbakht A, Khajedaluee M. Relationship between systemic lupus erythematosus disease activity index scores and subclinical cardiac problems. Iran Red Crescent Med J 2016;18:e38045.
38. Albayrak N, Bayram NA, Erten S, Sari C, Keles T, Durmaz T, Bastug S, Bozkurt E. The effects of undifferentiated spondyloarthropathy on left ventricular systolic and diastolic function. Int J Rheum Dis 2013;16:162-167.
39. Bayram NA, Cicek OF, Erten S, Keles T, Durmaz T, Bilen E, Sarı C, Bozkurt E. Assessment of left ventricular functions in patients with Sjögren's syndrome using tissue Doppler echocardiography. Int J Rheum Dis 2013;16:425-429.
40. Chen Y, Chung HY, Zhao CT, Wong A, Zhen Z, Tsang HH, Lau CS, Tse HF, Yiu KH. Left ventricular myocardial dysfunction and premature atherosclerosis in patients with axial spondyloarthritis. Rheumatology (Oxford) 2015;54:292-301.
41. Sveälv BG, Täng MS, Klingberg E, Forsblad-d'Elia H, Bergfeldt L. Prevalence of diastolic dysfunction in patients with ankylosing spondylitis: a cross-sectional study. Scand J Rheumatol 2015;44:111-117.
42. Heslinga SC, Van Dongen CJ, Konings TC, Peters MJ, Van der Horst-Bruinsma IE, Smulders YM, Nurmohamed MT. Diastolic left ventricular dysfunction in ankylosing spondylitis--a systematic review and meta-analysis. Semin Arthritis Rheum 2014;44:14-19.
| Files | ||
| Issue | Vol 15 No 2 (2020): J Teh Univ Heart Ctr | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/jthc.v15i2.4182 | |
| Keywords | ||
| Spondylitis; ankylosing Echocardiography Electrocardiography Ventricular dysfunction Heart block Aortic valve insufficiency | ||
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How to Cite
1.
Almasi S, Farahani B, Samiei N, Rezaei Y, Mahmoodi H, Qorbani M. Echocardiographic and Electrocardiographic Findings in Patients with Ankylosing Spondylitis without Cardiovascular Risk Factors. J Tehran Heart Cent. 2020;15(2):43-49.
