Advertisement

The International Journal of Cardiovascular Imaging

, Volume 35, Issue 9, pp 1637–1649 | Cite as

Right atrial function for the prediction of prognosis in connective tissue disease-associated pulmonary arterial hypertension: a study with two-dimensional speckle tracking

  • Yang Bai
  • Jun YangEmail author
  • Juanjuan Liu
  • Hongxia Ning
  • Rong Zhang
Original Paper

Abstract

Pulmonary arterial hypertension (PAH) is a serious and often fatal complication of connective tissue disease (CTD). Right atrial (RA) function is essential to maintaining adequate total right heart function in PAH. However, little is known about prognostic utility of RA function in CTD-PAH. RA longitudinal strain (LS) and strain rate (LSR) were evaluated in 53 consecutive patients (51 female, mean age 42 ± 15 years) with CTD-PAH, including systemic lupus erythematosus (SLE) (33.7%), mixed connective tissue disease (MCTD) (32.1%), primary Sjögren’s syndrome (pSS) (26.4%), and systemic sclerosis (SSc) (3.8%). At a mean follow-up of 19.3 ± 10.9 months, 20 patients (37.7%) were clinically worse. The group with clinical events had worse clinical conditions and poorer RA function at baseline compared with the group that had no clinical events. RA LS independently reflected World Health Organization functional class (WHO FC) after adjusting for RA area (RAA), tricuspid regurgitation (TR) grade, right ventricular (RV) global longitudinal strain (GLS), and pulmonary vascular resistance (PVR) (P = 0.006). Receiver operator characteristic (ROC) curve analysis indicated that RA LS < 22.9% was predictive of clinical worsening during follow-up (sensitivity = 80%; specificity = 87.9%; area under the curve (AUC) = 0.858), and the Kaplan–Meier curve confirmed that RA LS ≥ 22.9% was associated with more favorable long-term outcomes compared to RA LS < 22.9% (log-rank P < 0.01). On univariate Cox proportional hazards analysis, PVR, RVGLS, RAA, and RA LS were associated with long-term outcome, while RA LS was the only independent predictor in the multivariate analysis. Our findings suggest that RA LS measurements by speckle-tracking echocardiography (STE) can independently reflect the extent of right heart failure and predict clinical outcomes in patients with CTD-PAH. RA LS < 22.9% is associated with a higher risk of clinical worsening.

Keywords

Pulmonary arterial hypertension Connective tissue disease Right atrium Strain Speckle tracking Echocardiography 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest for this work.

References

  1. 1.
    Steen VD, Medsger TA (2007) Changes in causes of death in systemic sclerosis, 1972–2002. Ann Rheum Dis 66(7):940–944.  https://doi.org/10.1136/ard.2006.066068 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Fei Y, Shi X, Gan F, Li X, Zhang W, Li M, Hou Y, Zhang X, Zhao Y, Zeng X, Zhang F (2014) Death causes and pathogens analysis of systemic lupus erythematosus during the past 26 years. Clin Rheumatol 33(1):57–63.  https://doi.org/10.1007/s10067-013-2383-3 CrossRefPubMedGoogle Scholar
  3. 3.
    McGoon MD, Miller DP (2012) REVEAL: a contemporary US pulmonary arterial hypertension registry. Eur Respir Rev 21(123):8–18.  https://doi.org/10.1183/09059180.00008211 CrossRefPubMedGoogle Scholar
  4. 4.
    McLaughlin VV, Presberg KW, Doyle RL, Abman SH, McCrory DC, Fortin T, Ahearn G (2004) Prognosis of pulmonary arterial hypertension: aCCP evidence-based clinical practice guidelines. Chest 126(1 Suppl):78S–92S.  https://doi.org/10.1378/chest.126.1_suppl.78S CrossRefPubMedGoogle Scholar
  5. 5.
    Sivak JA, Raina A, Forfia PR (2016) Assessment of the physiologic contribution of right atrial function to total right heart function in patients with and without pulmonary arterial hypertension. Pulm Circ 6(3):322–328.  https://doi.org/10.1086/687767 CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Sachdev A, Villarraga HR, Frantz RP, McGoon MD, Hsiao JF, Maalouf JF, Ammash NM, McCully RB, Miller FA, Pellikka PA, Oh JK, Kane GC (2011) Right ventricular strain for prediction of survival in patients with pulmonary arterial hypertension. Chest 139(6):1299–1309.  https://doi.org/10.1378/chest.10-2015 CrossRefPubMedGoogle Scholar
  7. 7.
    Querejeta Roca G, Campbell P, Claggett B, Solomon SD, Shah AM (2015) Right atrial function in pulmonary arterial hypertension. Circ Cardiovasc Imaging 8(11):e003521.  https://doi.org/10.1161/circimaging.115.003521 (discussion e003521) CrossRefPubMedGoogle Scholar
  8. 8.
    Bhave NM, Visovatti SH, Kulick B, Kolias TJ, McLaughlin VV (2017) Right atrial strain is predictive of clinical outcomes and invasive hemodynamic data in group 1 pulmonary arterial hypertension. Int J Cardiovasc Imaging 33(6):847–855.  https://doi.org/10.1007/s10554-017-1081-7 CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Liu W, Wang Y, Zhou J, Bai H, Wang F, Wang J (2018) The association of functional capacity with right atrial deformation in patients with pulmonary arterial hypertension: a study with two-dimensional speckle tracking. Heart Lung Circ 27(3):350–358.  https://doi.org/10.1016/j.hlc.2017.02.029 CrossRefPubMedGoogle Scholar
  10. 10.
    Kato M, Atsumi T (2018) Pulmonary arterial hypertension associated with connective tissue diseases: a review focusing on distinctive clinical aspects. Eur J Clin Invest.  https://doi.org/10.1111/eci.12876 CrossRefPubMedGoogle Scholar
  11. 11.
    Huang C, Zhang S, Tian Z, Li M, Zeng X (2014) Could pulmonary arterial hypertension be an active index of systemic lupus erythematosus? A successful case of SLE-PAH cured by methylprednisolone pulse therapy. Lupus 23(14):1533–1536.  https://doi.org/10.1177/0961203314552461 CrossRefPubMedGoogle Scholar
  12. 12.
    Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, Lancellotti P, Muraru D, Picard MH, Rietzschel ER, Rudski L, Spencer KT, Tsang W, Voigt JU (2015) Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging 16(3):233–270.  https://doi.org/10.1093/ehjci/jev014 CrossRefPubMedGoogle Scholar
  13. 13.
    Nagueh SF, Smiseth OA, Appleton CP, Byrd BF 3rd, Dokainish H, Edvardsen T, Flachskampf FA, Gillebert TC, Klein AL, Lancellotti P, Marino P, Oh JK, Popescu BA, Waggoner AD (2016) Recommendations for the evaluation of left ventricular diastolic function by echocardiography: an update from the american society of echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiogr 29(4):277–314.  https://doi.org/10.1016/j.echo.2016.01.011 CrossRefPubMedGoogle Scholar
  14. 14.
    Rudski LG, Lai WW, Afilalo J, Hua L, Handschumacher MD, Chandrasekaran K, Solomon SD, Louie EK, Schiller NB (2010) Guidelines for the echocardiographic assessment of the right heart in adults: a report from the American Society of Echocardiography endorsed by the European Association of Echocardiography, a registered branch of the European Society of Cardiology, and the Canadian Society of Echocardiography. J Am Soc Echocardiogr 23(7):685–713.  https://doi.org/10.1016/j.echo.2010.05.010 (quiz 786-688) CrossRefPubMedGoogle Scholar
  15. 15.
    Galie N, Humbert M, Vachiery JL, Gibbs S, Lang I, Torbicki A, Simonneau G, Peacock A, Vonk Noordegraaf A, Beghetti M, Ghofrani A, Gomez Sanchez MA, Hansmann G, Klepetko W, Lancellotti P, Matucci M, McDonagh T, Pierard LA, Trindade PT, Zompatori M, Hoeper M, Group ESCSD (2016) 2015 ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension: the Joint Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS): Endorsed by: Association for European Paediatric and Congenital Cardiology (AEPC), International Society for Heart and Lung Transplantation (ISHLT). Eur Heart J 37(1):67–119.  https://doi.org/10.1093/eurheartj/ehv317 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Chemla D, Castelain V, Humbert M, Hebert JL, Simonneau G, Lecarpentier Y, Herve P (2004) New formula for predicting mean pulmonary artery pressure using systolic pulmonary artery pressure. Chest 126(4):1313–1317.  https://doi.org/10.1378/chest.126.4.1313 CrossRefPubMedGoogle Scholar
  17. 17.
    Opotowsky AR, Clair M, Afilalo J, Landzberg MJ, Waxman AB, Moko L, Maron BA, Vaidya A, Forfia PR (2013) A simple echocardiographic method to estimate pulmonary vascular resistance. Am J Cardiol 112(6):873–882.  https://doi.org/10.1016/j.amjcard.2013.05.016 CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Chung L, Liu J, Parsons L, Hassoun PM, McGoon M, Badesch DB, Miller DP, Nicolls MR, Zamanian RT (2010) Characterization of connective tissue disease-associated pulmonary arterial hypertension from REVEAL: identifying systemic sclerosis as a unique phenotype. Chest 138(6):1383–1394.  https://doi.org/10.1378/chest.10-0260 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Humbert M, Sitbon O, Chaouat A, Bertocchi M, Habib G, Gressin V, Yaici A, Weitzenblum E, Cordier JF, Chabot F, Dromer C, Pison C, Reynaud-Gaubert M, Haloun A, Laurent M, Hachulla E, Simonneau G (2006) Pulmonary arterial hypertension in France: results from a national registry. Am J Respir Crit Care Med 173(9):1023–1030.  https://doi.org/10.1164/rccm.200510-1668OC CrossRefPubMedGoogle Scholar
  20. 20.
    Shirai Y, Yasuoka H, Okano Y, Takeuchi T, Satoh T, Kuwana M (2012) Clinical characteristics and survival of Japanese patients with connective tissue disease and pulmonary arterial hypertension: a single-centre cohort. Rheumatology (Oxford, England) 51(10):1846–1854.  https://doi.org/10.1093/rheumatology/kes140 CrossRefGoogle Scholar
  21. 21.
    Hao YJ, Jiang X, Zhou W, Wang Y, Gao L, Wang Y, Li GT, Hong T, Huo Y, Jing ZC, Zhang ZL (2014) Connective tissue disease-associated pulmonary arterial hypertension in Chinese patients. Eur Respir J 44(4):963–972.  https://doi.org/10.1183/09031936.00182813 CrossRefPubMedGoogle Scholar
  22. 22.
    Miyamichi-Yamamoto S, Fukumoto Y, Sugimura K, Ishii T, Satoh K, Miura Y, Tatebe S, Nochioka K, Aoki T, Do EZ, Shimokawa H (2011) Intensive immunosuppressive therapy improves pulmonary hemodynamics and long-term prognosis in patients with pulmonary arterial hypertension associated with connective tissue disease. Circ J 75(11):2668–2674CrossRefPubMedGoogle Scholar
  23. 23.
    Sanchez O, Sitbon O, Jais X, Simonneau G, Humbert M (2006) Immunosuppressive therapy in connective tissue diseases-associated pulmonary arterial hypertension. Chest 130(1):182–189.  https://doi.org/10.1378/chest.130.1.182 CrossRefPubMedGoogle Scholar
  24. 24.
    Johnson SR, Granton JT (2011) Pulmonary hypertension in systemic sclerosis and systemic lupus erythematosus. Eur Respir Rev 20(122):277–286.  https://doi.org/10.1183/09059180.00003811 CrossRefPubMedGoogle Scholar
  25. 25.
    D’Andrea A, D’Alto M, Di Maio M, Vettori S, Benjamin N, Cocchia R, Argiento P, Romeo E, Di Marco G, Russo MG, Valentini G, Calabro R, Bossone E, Grunig E (2016) Right atrial morphology and function in patients with systemic sclerosis compared to healthy controls: a two-dimensional strain study. Clin Rheumatol 35(7):1733–1742.  https://doi.org/10.1007/s10067-016-3279-9 CrossRefPubMedGoogle Scholar
  26. 26.
    Ge XY, Shao L, Zheng ZL (2016) Assessment right atrial function in patients with systemic lupus erythematosus by speckle tracking and three-dimensional echocardiography. Zhonghua yi xue za zhi 96(47):3815–3818.  https://doi.org/10.3760/cma.j.issn.0376-2491.2016.47.010 CrossRefPubMedGoogle Scholar
  27. 27.
    Rai AB, Lima E, Munir F, Faisal Khan A, Waqas A, Bughio S, ul Haq E, Attique HB, Rahman ZU (2015) Speckle tracking echocardiography of the right atrium: the neglected chamber. Clin Cardiol 38(11):692–697.  https://doi.org/10.1002/clc.22438 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Deng Y, Guo SL, Wu WF, Wang Q, Su HY, Tan Z, Wang F, He QY (2016) Right atrial evaluation in patients with pulmonary hypertension: a real-time 3-dimensional transthoracic echocardiographic study. J Ultrasound Med 35(1):49–61.  https://doi.org/10.7863/ultra.15.01028 CrossRefPubMedGoogle Scholar
  29. 29.
    D’Alto M, D’Andrea A, Di Salvo G, Scognamiglio G, Argiento P, Romeo E, Di Marco GM, Mattera Iacono A, Bossone E, Sarubbi B, Russo MG (2017) Right atrial function and prognosis in idiopathic pulmonary arterial hypertension. Int J Cardiol 248:320–325.  https://doi.org/10.1016/j.ijcard.2017.08.047 CrossRefPubMedGoogle Scholar
  30. 30.
    Gan CT, Holverda S, Marcus JT, Paulus WJ, Marques KM, Bronzwaer JG, Twisk JW, Boonstra A, Postmus PE, Vonk-Noordegraaf A (2007) Right ventricular diastolic dysfunction and the acute effects of sildenafil in pulmonary hypertension patients. Chest 132(1):11–17.  https://doi.org/10.1378/chest.06-1263 CrossRefPubMedGoogle Scholar
  31. 31.
    Gaynor SL, Maniar HS, Prasad SM, Steendijk P, Moon MR (2005) Reservoir and conduit function of right atrium: impact on right ventricular filling and cardiac output. Am J Physiol Heart Circ Physiol 288(5):H2140–2145.  https://doi.org/10.1152/ajpheart.00566.2004 CrossRefPubMedGoogle Scholar
  32. 32.
    Hoit BD, Gabel M (2000) Influence of left ventricular dysfunction on the role of atrial contraction: an echocardiographic-hemodynamic study in dogs. J Am Coll Cardiol 36(5):1713–1719CrossRefPubMedGoogle Scholar
  33. 33.
    Sato T, Tsujino I, Oyama-Manabe N, Ohira H, Ito YM, Yamada A, Ikeda D, Watanabe T, Nishimura M (2013) Right atrial volume and phasic function in pulmonary hypertension. Int J Cardiol 168(1):420–426.  https://doi.org/10.1016/j.ijcard.2012.09.133 CrossRefPubMedGoogle Scholar
  34. 34.
    Anwar AM, Geleijnse ML, Soliman OI, Nemes A, ten Cate FJ (2007) Left atrial Frank-Starling law assessed by real-time, three-dimensional echocardiographic left atrial volume changes. Heart 93(11):1393–1397.  https://doi.org/10.1136/hrt.2006.099366 CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Patel AR, Alsheikh-Ali AA, Mukherjee J, Evangelista A, Quraini D, Ordway LJ, Kuvin JT, Denofrio D, Pandian NG (2011) 3D echocardiography to evaluate right atrial pressure in acutely decompensated heart failure correlation with invasive hemodynamics. JACC Cardiovasc Imaging 4(9):938–945.  https://doi.org/10.1016/j.jcmg.2011.05.006 CrossRefPubMedGoogle Scholar
  36. 36.
    Sato T, Tsujino I, Ohira H, Oyama-Manabe N, Ito YM, Yamada A, Ikeda D, Watanabe T, Nishimura M (2015) Right atrial volume and reservoir function are novel independent predictors of clinical worsening in patients with pulmonary hypertension. J Heart Lung Transplant 34(3):414–423.  https://doi.org/10.1016/j.healun.2015.01.984 CrossRefPubMedGoogle Scholar
  37. 37.
    Darsaklis K, Dickson ME, Cornwell W 3rd, Ayers CR, Torres F, Chin KM, Matulevicius S (2016) Right atrial emptying fraction non-invasively predicts mortality in pulmonary hypertension. Int J Cardiovasc Imaging 32(7):1121–1130.  https://doi.org/10.1007/s10554-016-0883-3 CrossRefPubMedGoogle Scholar
  38. 38.
    Brunner NW, Haddad F, Kobayashi Y, Hsi A, Swiston JR, Gin KG, Zamanian RT (2015) Prognostic utility of right atrial emptying fractions in pulmonary arterial hypertension. Pulm Circ 5(3):473–480.  https://doi.org/10.1086/682218 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Fukuda Y, Tanaka H, Ryo-Koriyama K, Motoji Y, Sano H, Shimoura H, Ooka J, Toki H, Sawa T, Mochizuki Y, Matsumoto K, Emoto N, Hirata K (2016) Comprehensive functional assessment of right-sided heart using speckle tracking strain for patients with pulmonary hypertension. Echocardiography 33(7):1001–1008.  https://doi.org/10.1111/echo.13205 CrossRefPubMedGoogle Scholar
  40. 40.
    Shukla M, Park JH, Thomas JD, Delgado V, Bax JJ, Kane GC, Howlett JG, White JA, Fine NM (2018) Prognostic value of right ventricular strain using speckle-tracking echocardiography in pulmonary hypertension: a systematic review and meta-analysis. Can J Cardiol 34(8):1069–1078.  https://doi.org/10.1016/j.cjca.2018.04.016 CrossRefPubMedGoogle Scholar
  41. 41.
    da Costa Junior AA, Ota-Arakaki JS, Ramos RP, Uellendahl M, Mancuso FJ, Gil MA, Fischer CH, Moises VA, de Camargo Carvalho AC, Campos O (2017) Diagnostic and prognostic value of right ventricular strain in patients with pulmonary arterial hypertension and relatively preserved functional capacity studied with echocardiography and magnetic resonance. Int J Cardiovasc Imaging 33(1):39–46.  https://doi.org/10.1007/s10554-016-0966-1 CrossRefPubMedGoogle Scholar
  42. 42.
    Campo A, Mathai SC, Le Pavec J, Zaiman AL, Hummers LK, Boyce D, Housten T, Lechtzin N, Chami H, Girgis RE, Hassoun PM (2011) Outcomes of hospitalisation for right heart failure in pulmonary arterial hypertension. Eur Respir J 38(2):359–367.  https://doi.org/10.1183/09031936.00148310 CrossRefPubMedGoogle Scholar
  43. 43.
    Peluso D, Badano LP, Muraru D, Dal Bianco L, Cucchini U, Kocabay G, Kovacs A, Casablanca S, Iliceto S (2013) Right atrial size and function assessed with three-dimensional and speckle-tracking echocardiography in 200 healthy volunteers. Eur Heart J Cardiovasc Imaging 14(11):1106–1114.  https://doi.org/10.1093/ehjci/jet024 CrossRefPubMedGoogle Scholar
  44. 44.
    Nemes A, Domsik P, Kalapos A, Kormanyos A, Ambrus N, Forster T (2018) Three-dimensional speckle-tracking echocardiography detects different patterns of right atrial dysfunction in selected disorders: a short summary from the MAGYAR-Path Study. Quant Imaging Med Surg 8(2):182–186.  https://doi.org/10.21037/qims.2018.01.11 CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Vitarelli A, Mangieri E, Gaudio C, Tanzilli G, Miraldi F, Capotosto L (2018) Right atrial function by speckle tracking echocardiography in atrial septal defect: prediction of atrial fibrillation. Clin Cardiol 41(10):1341–1347.  https://doi.org/10.1002/clc.23051 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Yang Bai
    • 1
  • Jun Yang
    • 1
    Email author
  • Juanjuan Liu
    • 1
  • Hongxia Ning
    • 1
  • Rong Zhang
    • 2
  1. 1.Department of Cardiovascular UltrasoundThe First Hospital of China Medical UniversityShenyangChina
  2. 2.Department of RheumatologyThe First Hospital of China Medical UniversityShenyangChina

Personalised recommendations