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12-05-2018 | Ankylosing spondylitis | Article

Assessment of aortic stiffness in patients with ankylosing spondylitis using cardiovascular magnetic resonance

Journal: Clinical Rheumatology

Authors: P. Stefan Biesbroek, Sjoerd C. Heslinga, Peter M. van de Ven, Mike J. L. Peters, Raquel P. Amier, Thelma C. Konings, Christopher D. Maroules, Colby Ayers, Parag H. Joshi, Irene E. van der Horst-Bruinsma, Vokko P. van Halm, Albert C. van Rossum, Michael T. Nurmohamed, Robin Nijveldt

Publisher: Springer London

Abstract

To evaluate aortic stiffness in patients with ankylosing spondylitis (AS) using cardiovascular magnetic resonance (CMR) and to assess its association with AS characteristics and left ventricular (LV) remodeling. In this prospective study, 14 consecutive AS patients were each matched to two controls without cardiovascular symptoms or known cardiovascular disease who underwent CMR imaging for the assessment of aortic arch pulse wave velocity (PWV) at 1.5 Tesla. To enhance comparability of the samples, matching was done with replacement resulting in 20 unique controls. Only AS patients with abnormal findings on screening echocardiography were included in this exploratory study. Cine CMR was used to assess LV geometry and systolic function, and late gadolinium enhancement was performed to determine the presence of myocardial hyperenhancement (i.e., fibrosis). Aortic arch PWV was significantly higher in the AS group compared with the control group (median 9.7 m/s, interquartile range [IQR] 7.1 to 11.8 vs. 6.1 m/s, IQR 4.6 to 7.6 m/s; p < 0.001). PWV was positively associated with functional disability as measured by BASFI (R: 0.62; p = 0.018). Three patients (21%) with a non-ischemic pattern of hyperenhancement showed increased PWV (11.7, 12.3, and 16.5 m/s) as compared to the 11 patients without hyperenhancement (9.0 m/s, IQR 6.6 to 10.5 m/s; p = 0.022). PWV was inversely associated with LV ejection fraction (R: − 0.63; p = 0.015), but was not found to be statistically correlated to LV volumes or mass. Aortic arch PWV was increased in our cohort of patients with AS. Higher PWV in the aortic arch was associated with functional disability, the presence of non-ischemic hyperenhancement, and reduced LV systolic function.
Literature
1.
Haroon NN, Paterson JM, Li P, Inman RD, Haroon N (2015) Patients With Ankylosing Spondylitis Have Increased Cardiovascular and Cerebrovascular Mortality: A Population-Based Study. Ann Intern Med 163(6):409–416. https://​doi.​org/​10.​7326/​M14-2470 CrossRefPubMed
2.
Heslinga SC, Van Dongen CJ, Konings TC, Peters MJ, Van der Horst-Bruinsma IE, Smulders YM, Nurmohamed MT (2014) Diastolic left ventricular dysfunction in ankylosing spondylitis--a systematic review and meta-analysis. Semin Arthritis Rheum 44(1):14–19. https://​doi.​org/​10.​1016/​j.​semarthrit.​2014.​02.​004 CrossRefPubMed
3.
Peters MJ, van Eijk IC, Smulders YM, Serne E, Dijkmans BA, van der Horst-Bruinsma IE, Nurmohamed MT (2010) Signs of accelerated preclinical atherosclerosis in patients with ankylosing spondylitis. J Rheumatol 37(1):161–166. https://​doi.​org/​10.​3899/​jrheum.​090667 CrossRefPubMed
4.
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 (2017) Insights into cardiac involvement in ankylosing spondylitis from cardiovascular magnetic resonance. Heart 103(10):745–752. https://​doi.​org/​10.​1136/​heartjnl-2016-310667 CrossRefPubMed
5.
Jain S, Khera R, Corrales-Medina VF, Townsend RR, Chirinos JA (2014) Inflammation and arterial stiffness in humans. Atherosclerosis 237(2):381–390. https://​doi.​org/​10.​1016/​j.​atherosclerosis.​2014.​09.​011 CrossRefPubMed
6.
Vlachopoulos C, Aznaouridis K, Stefanadis C (2010) Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol 55(13):1318–1327. https://​doi.​org/​10.​1016/​j.​jacc.​2009.​10.​061 CrossRefPubMed
7.
Laurent S, Cockcroft J, Van Bortel L, Boutouyrie P, Giannattasio C, Hayoz D, Pannier B, Vlachopoulos C, Wilkinson I, Struijker-Boudier H, European Network for Non-invasive Investigation of Large A (2006) Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J 27(21):2588–2605. https://​doi.​org/​10.​1093/​eurheartj/​ehl254 CrossRefPubMed
8.
Avram C, Dragoi RG, Popoviciu H, Dragoi M, Avram A, Amaricai E (2016) Association between arterial stiffness, disease activity and functional impairment in ankylosing spondylitis patients: a cross-sectional study. Clin Rheumatol 35(8):2017–2022. https://​doi.​org/​10.​1007/​s10067-016-3297-7 CrossRefPubMed
9.
Bodnar N, Kerekes G, Seres I, Paragh G, Kappelmayer J, Nemethne ZG, Szegedi G, Shoenfeld Y, Sipka S, Soltesz P, Szekanecz Z, Szanto S (2011) Assessment of subclinical vascular disease associated with ankylosing spondylitis. J Rheumatol 38(4):723–729. https://​doi.​org/​10.​3899/​jrheum.​100668 CrossRefPubMed
10.
Arida A, Protogerou AD, Konstantonis G, Konsta M, Delicha EM, Kitas GD, Sfikakis PP (2015) Subclinical atherosclerosis is not accelerated in patients with Ankylosing spondylitis with low disease activity: new data and Metaanalysis of published studies. J Rheumatol 42(11):2098–2105. https://​doi.​org/​10.​3899/​jrheum.​150316 CrossRefPubMed
11.
Berg IJ, van der Heijde D, Dagfinrud H, Seljeflot I, Olsen IC, Kvien TK, Semb AG, Provan SA (2015) Disease activity in ankylosing spondylitis and associations to markers of vascular pathology and traditional cardiovascular disease risk factors: a cross-sectional study. J Rheumatol 42(4):645–653. https://​doi.​org/​10.​3899/​jrheum.​141018 CrossRefPubMed
12.
Grotenhuis HB, Westenberg JJ, Steendijk P, van der Geest RJ, Ottenkamp J, Bax JJ, Jukema JW, de Roos A (2009) Validation and reproducibility of aortic pulse wave velocity as assessed with velocity-encoded MRI. J Magn Reson Imaging 30(3):521–526. https://​doi.​org/​10.​1002/​jmri.​21886 CrossRefPubMed
13.
Ohyama Y, Ambale-Venkatesh B, Noda C, Chugh AR, Teixido-Tura G, Kim JY, Donekal S, Yoneyama K, Gjesdal O, Redheuil A, Liu CY, Nakamura T, Wu CO, Hundley WG, Bluemke DA, Lima JA (2016) Association of Aortic Stiffness with Left Ventricular Remodeling and Reduced Left Ventricular Function Measured by magnetic resonance imaging: the multi-ethnic study of atherosclerosis. Circ Cardiovasc Imaging 9(7):e004426. https://​doi.​org/​10.​1161/​CIRCIMAGING.​115.​004426 CrossRefPubMed
14.
van der Linden S, Valkenburg HA, Cats A (1984) Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheumatol 27(4):361–368CrossRef
15.
Maroules CD, Khera A, Ayers C, Goel A, Peshock RM, Abbara S, King KS (2014) Cardiovascular outcome associations among cardiovascular magnetic resonance measures of arterial stiffness: the Dallas heart study. J Cardiovasc Magn Reson 16:33. https://​doi.​org/​10.​1186/​1532-429X-16-33 CrossRefPubMedPubMedCentral
16.
Stuart EA (2010) Matching methods for causal inference: a review and a look forward. Stat Sci 25(1):1–21CrossRefPubMedPubMedCentral
17.
van der Heijde D, Lie E, Kvien TK, Sieper J, Van den Bosch F, Listing J, Braun J, Landewe R, Assessment of SpondyloArthritis international S (2009) ASDAS, a highly discriminatory ASAS-endorsed disease activity score in patients with ankylosing spondylitis. Ann Rheum Dis 68(12):1811–1818. https://​doi.​org/​10.​1136/​ard.​2008.​100826 CrossRefPubMed
18.
Calin A, Garrett S, Whitelock H, Kennedy LG, O'Hea J, Mallorie P, Jenkinson T (1994) A new approach to defining functional ability in ankylosing spondylitis: the development of the bath Ankylosing spondylitis functional index. J Rheumatol 21(12):2281–2285PubMed
19.
Jenkinson TR, Mallorie PA, Whitelock HC, Kennedy LG, Garrett SL, Calin A (1994) Defining spinal mobility in ankylosing spondylitis (AS). The bath AS metrology index. J Rheumatol 21(9):1694–1698PubMed
20.
Euser AM, Dekker FW, le Cessie S (2008) A practical approach to bland-Altman plots and variation coefficients for log transformed variables. J Clin Epidemiol 61(10):978–982. https://​doi.​org/​10.​1016/​j.​jclinepi.​2007.​11.​003 CrossRefPubMed
21.
Abadie A, Drukker D, Herr JL, Imbens GW (2004) Implementing matching estimators for average treatment effects in Stata. Stata J 4:290–311 %@ 1536-1867X
22.
Noda C, Ambale Venkatesh B, Ohyama Y, Liu CY, Chamera E, Redheuil A, Teixido-Tura G, Chugh AR, Wu CO, Hundley GW, Bluemke DA, Lima JA (2016) Reproducibility of functional aortic analysis using magnetic resonance imaging: the MESA. Eur Heart J Cardiovasc Imaging 17(8):909–917. https://​doi.​org/​10.​1093/​ehjci/​jev215 CrossRefPubMed
23.
Kerekes G, Soltesz P, Nurmohamed MT, Gonzalez-Gay MA, Turiel M, Vegh E, Shoenfeld Y, McInnes I, Szekanecz Z (2012) Validated methods for assessment of subclinical atherosclerosis in rheumatology. Nat Rev Rheumatol 8(4):224–234. https://​doi.​org/​10.​1038/​nrrheum.​2012.​16 CrossRefPubMed
24.
Krasnokutsky S, Romero AG, Bang D, Pike VC, Shah B, Igel TF, Dektiarev I, Guo Y, Zhong J, Katz SD, Pillinger MH (2018) Impaired arterial responsiveness in untreated gout patients compared with healthy non-gout controls: association with serum urate and C-reactive protein. Clin Rheumatol. https://​doi.​org/​10.​1007/​s10067-018-4029-y
25.
Rongen GA, van Ingen I, Kok M, Vonkeman H, Janssen M, Jansen TL (2018) Vasodilator function worsens after cessation of tumour necrosis factor inhibitor therapy in patients with rheumatoid arthritis only if a flare occurs. Clin Rheumatol 37(4):909–916. https://​doi.​org/​10.​1007/​s10067-017-3961-6 CrossRefPubMed
26.
Waring WS, McKnight JA, Webb DJ, Maxwell SR (2006) Uric acid restores endothelial function in patients with type 1 diabetes and regular smokers. Diabetes 55(11):3127–3132. https://​doi.​org/​10.​2337/​db06-0283 CrossRefPubMed
27.
Shahin Y, Khan JA, Chetter I (2012) Angiotensin converting enzyme inhibitors effect on arterial stiffness and wave reflections: a meta-analysis and meta-regression of randomised controlled trials. Atherosclerosis 221(1):18–33. https://​doi.​org/​10.​1016/​j.​atherosclerosis.​2011.​12.​005 CrossRefPubMed
28.
Ashor AW, Lara J, Siervo M, Celis-Morales C, Mathers JC (2014) Effects of exercise modalities on arterial stiffness and wave reflection: a systematic review and meta-analysis of randomized controlled trials. PLoS One 9(10):e110034. https://​doi.​org/​10.​1371/​journal.​pone.​0110034 CrossRefPubMedPubMedCentral
29.
Agnoletti G, Ou P, Celermajer DS, Boudjemline Y, Marini D, Bonnet D, Aggoun Y (2008) Acute angulation of the aortic arch predisposes a patient to ascending aortic dilatation and aortic regurgitation late after the arterial switch operation for transposition of the great arteries. J Thorac Cardiovasc Surg 135(3):568–572. https://​doi.​org/​10.​1016/​j.​jtcvs.​2007.​10.​020 CrossRefPubMed
30.
Murgo JP, Westerhof N, Giolma JP, Altobelli SA (1980) Aortic input impedance in normal man: relationship to pressure wave forms. Circulation 62(1):105–116CrossRefPubMed
31.
Schillaci G, Mannarino MR, Pucci G, Pirro M, Helou J, Savarese G, Vaudo G, Mannarino E (2007) Age-specific relationship of aortic pulse wave velocity with left ventricular geometry and function in hypertension. Hypertension 49(2):317–321. https://​doi.​org/​10.​1161/​01.​HYP.​0000255790.​98391.​9b CrossRefPubMed
32.
Ntusi NA, Piechnik SK, Francis JM, Ferreira VM, Matthews PM, Robson MD, Wordsworth PB, Neubauer S, Karamitsos TD (2015) Diffuse myocardial fibrosis and inflammation in rheumatoid arthritis: insights from CMR T1 mapping. JACC Cardiovasc Imaging 8(5):526–536. https://​doi.​org/​10.​1016/​j.​jcmg.​2014.​12.​025 CrossRefPubMed
33.
Seneviratne MG, Grieve SM, Figtree GA, Garsia R, Celermajer DS, Adelstein S, Puranik R (2016) Prevalence, distribution and clinical correlates of myocardial fibrosis in systemic lupus erythematosus: a cardiac magnetic resonance study. Lupus 25(6):573–581. https://​doi.​org/​10.​1177/​0961203315622275​ CrossRefPubMed
34.
Ntusi NA, Piechnik SK, Francis JM, Ferreira VM, Rai AB, Matthews PM, Robson MD, Moon J, Wordsworth PB, Neubauer S, Karamitsos TD (2014) Subclinical myocardial inflammation and diffuse fibrosis are common in systemic sclerosis--a clinical study using myocardial T1-mapping and extracellular volume quantification. J Cardiovasc Magn Reson 16:21. https://​doi.​org/​10.​1186/​1532-429X-16-21 CrossRefPubMedPubMedCentral
35.
Karp G, Wolak A, Baumfeld Y, Bar-Am N, Novack V, Wolak T, Fuchs L, Shalev A, Shelef I, Abu-Shakra M (2016) Assessment of aortic stiffness among patients with systemic lupus erythematosus and rheumatoid arthritis by magnetic resonance imaging. Int J Cardiovasc Imaging 32(6):935–944. https://​doi.​org/​10.​1007/​s10554-016-0851-y CrossRefPubMed
36.
Rudolph A, Abdel-Aty H, Bohl S, Boye P, Zagrosek A, Dietz R, Schulz-Menger J (2009) Noninvasive detection of fibrosis applying contrast-enhanced cardiac magnetic resonance in different forms of left ventricular hypertrophy relation to remodeling. J Am Coll Cardiol 53(3):284–291. https://​doi.​org/​10.​1016/​j.​jacc.​2008.​08.​064 CrossRefPubMed
37.
Kuznetsova T, Herbots L, Lopez B, Jin Y, Richart T, Thijs L, Gonzalez A, Herregods MC, Fagard RH, Diez J, Staessen JA (2009) Prevalence of left ventricular diastolic dysfunction in a general population. Circ Heart Fail 2(2):105–112. https://​doi.​org/​10.​1161/​CIRCHEARTFAILURE​.​108.​822627 CrossRefPubMed
38.
Rolf MP, Hofman MB, Gatehouse PD, Markenroth-Bloch K, Heymans MW, Ebbers T, Graves MJ, Totman JJ, Werner B, van Rossum AC, Kilner PJ, Heethaar RM (2011) Sequence optimization to reduce velocity offsets in cardiovascular magnetic resonance volume flow quantification--a multi-vendor study. J Cardiovasc Magn Reson 13:18. https://​doi.​org/​10.​1186/​1532-429X-13-18 CrossRefPubMedPubMedCentral