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Assessment of biventricular systolic strain derived from the two-dimensional and three-dimensional speckle tracking echocardiography in lymphoma patients after anthracycline therapy

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Abstract

The aim of this study was to investigate the usefulness of three-dimensional (3D) speckle tracking echocardiography (STE) for assessment of both left and right ventricular systolic function in patients with lymphoma after anthracycline chemotherapy, compared with two-dimensional (2D) STE. Totally eighty-nine patients undergoing anthracycline containing chemotherapy were studied. Echocardiographic assessment included 2D and 3D left ventricular (LV) global longitudinal strain (GLS), global circumferential strain (GCS) and right ventricular (RV) GLS. All the parameters were analyzed at baseline, after the completion of four cycles and at the end of the regimen respectively. The area under the receiver operating characteristic curve was calculated to determine the capability of various echocardiographic parameters to discriminate between before and after chemotherapy. Compared with those at baseline, the 3D GLS and GCS of LV and GLS of RV decreased significantly after four cycles of the therapy (all p < 0.01). At the end of the treatment, 2D GLS and GCS of LV deteriorated markedly (both p < 0.05). The area under the curve for GLS, GCS of LV and GLS of RV derived by 3D were 0.81, 0.66 and 0.78, respectively. The cutoff value with −20.4% of LV GLS by 3D had sensitivity of 81% and specificity of 66% for differentiating patients after therapy from baselines. The cutoff value with −21.9% of RV GLS by 3D had sensitivity of 71% and specificity of 74% fordifferentiating patients after therapy from baselines. The data from this study demonstrated that both 2D and 3D STE can be conducted to evaluate the slight myocardial damage for lymphoma patients after anthracycline chemotherapy. 3D STE could examine subclinical biventricular dysfunction in earlier point than 2D STE.

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References

  1. Karakurt C, Çelik S, Selimoğlu A, Varol I, Karabiber H, Yoloğlu S (2016) Strain and strain rate echocardiography in children with Wilson’s disease. Cardiovasc J Afr 27:1–8

    Article  Google Scholar 

  2. Li VW, Cheuk DK, Cheng FW, Yang JY, Yau JP, Ho KK, Li CK, Li RC, Yuen HL, Ling AS, Chan GC, Cheung YF (2016) Myocardial stiffness as assessed by diastolic wall strain in adult survivors of childhood leukaemias with preserved left ventricular ejection fraction. Eur Heart J Cardiovasc Imaging

  3. Lemarié J, Huttin O, Girerd N, Mandry D, Juillière Y, Moulin F, Lemoine S, Beaumont M, Marie PY, Selton-Suty C (2015) Usefulness of speckle-tracking imaging for right ventricular assessment after acute myocardial infarction: a magnetic resonance imaging/echocardiographic comparison within the relation between aldosterone and cardiac remodeling after myocardial infarction study. J Am Soc Echocardiogr 28(7):818–827

    Article  PubMed  Google Scholar 

  4. Lu KJ, Chen JX, Profitis K, Kearney LG, DeSilva D, Smith G, Ord M, Harberts S, Calafiore P, Jones E, Srivastava PM (2015) Right ventricular global longitudinal strain is an independent predictor of right ventricular function: a multimodality study of cardiac magnetic resonance imaging, real time three-dimensional echocardiography and speckle tracking echocardiography. Echocardiography 32(6):966–974

    Article  PubMed  Google Scholar 

  5. Lange SA, Jung J, Jaeck A, Hitschold T, Ebner B (2016) Subclinical myocardial impairment occurred in septal and anterior LV wall segments after anthracycline-embedded chemotherapy and did not worsen during adjuvant trastuzumab treatment in breast cancer patients. Cardiovasc Toxicol 16(2):193–206

    Article  CAS  PubMed  Google Scholar 

  6. Agha H, Shalaby L, Attia W, Abdelmohsen G, Aziz OA, Rahman MY (2016) Early ventricular dysfunction after anthracycline chemotherapy in children. Pediatr Cardiol 37(3):537–544

    Article  PubMed  Google Scholar 

  7. Ali MT, Yucel E, Bouras S, Wang L, Fei HW, Halpern EF, Scherrer-Crosbie M (2016) Myocardial strain is associated with adverse clinical cardiac events in patients treated with anthracyclines. J Am Soc Echocardiogr 29:522–527

    Article  PubMed  Google Scholar 

  8. Calleja A, Poulin F, Khorolsky C, Shariat M, Bedard PL, Amir E, Rakowski H, McDonald M, Delgado D, Thavendiranathan P (2015) Right ventricular dysfunction in patients experiencing cardiotoxicity during breast cancer therapy. J Oncol X. doi:10.1155/2015/609194

    Google Scholar 

  9. Spratt JR, Raveendran G, Liao K, John R (2016) Novel techniques in stress echocardiography: a focus on the advantages and disadvantages. Expert Rev Cardiovasc 14(4):477–494. doi:10.1586/14779072.2016.1135054

    Article  Google Scholar 

  10. Ostenfeld E, A Flachskampf F (2015) Assessment of right ventricular volumes and ejection fraction by echocardiography: from geometric approximations to realistic shapes. Echo Res Pract 2(1):R1–R11. doi:10.1530/ERP-14-0077

    Article  PubMed  PubMed Central  Google Scholar 

  11. Lang RM, Badano LP, Tsang W et al (2012) EAE/ASE recommendations for image acquisition and display using three-dimensional echocardiography. J Am Soc Echocardiogr 13(1):1–46. doi:10.1093/ehjci/jer316

    Google Scholar 

  12. Lang RM, Bierig M, Devereux RB et al (2006) American Society of Echocardiography’s Nomenclature and Standards Committee, Task Force on Chamber Quantification, American College of Cardiology Echocardiography Committee, American Heart Association, European Association of Echocardiography, European Society of Cardiology. Recommendations for chamber quantification. Eur J Echocardiogr 7(2):79–108

    Article  PubMed  Google Scholar 

  13. Freund Y, Chenevier-Gobeaux C, Bonnet P, Claessens YE, Allo JC, Doumenc B, Leumani F, Cosson C, Riou B, Ray P (2011) High-sensitivity versus conventional troponin in the emergency department for the diagnosis of acute myocardial infarction. Crit Care 15(3):R147. doi:10.1186/cc10270

    Article  PubMed  PubMed Central  Google Scholar 

  14. Martín M, Esteva FJ, Alba E, Khandheria B, Pérez-Isla L, García-Sáenz JA, Márquez A, Sengupta P, Zamorano J (2009) Minimizing cardiotoxicity while optimizing treatment efficacy with trastuzumab: review and expert recommendations. Oncologist 14(1):1–11. doi:10.1634/theoncologist.2008-0137

    Article  PubMed  Google Scholar 

  15. Otsuka T, Kawada T, Ibuki C, Seino Y (2010) Association between high-sensitivity cardiac troponin T levels and the predicted cardiovascular risk in middle-aged men without overt cardiovascular disease. Am Heart J 159(6):972–978. doi:10.1016/j.ahj.2010.02.036

    Article  CAS  PubMed  Google Scholar 

  16. DeSantis CE, Lin CC, Mariotto AB, Siegel RL, Stein KD, Kramer JL, Alteri R, Robbins AS, Jemal A (2014) Cancer treatment and survivorship statistics, 2014. CA Cancer J Clin 64(4):252–271. doi:10.3322/caac21235

    Article  PubMed  Google Scholar 

  17. Tukenova M, Guibout C, Oberlin O, Doyon F, Mousannif A, Haddy N, Guérin S, Pacquement H, Aouba A, Hawkins M, Winter D, Bourhis J, Lefkopoulos D, Diallo I, de Vathaire F (2010) Role of cancer treatment in long-term overall and cardiovascular mortality after childhood cancer. J Clin Oncol 28(8):1308–1315. doi:10.1200/JCO.2008.20.2267

    Article  PubMed  Google Scholar 

  18. Mertens AC, Liu Q, Neglia JP, Wasilewski K, Leisenring W, Armstrong GT, Robison LL, Yasui Y (2008) Cause-specific late mortality among 5-year survivors of childhood cancer: the Childhood Cancer Survivor Study. J Natl Cancer Inst 100(19):1368–1379. doi:10.1093/jnci/djn310

    Article  PubMed  PubMed Central  Google Scholar 

  19. Monsuez JJ, Charniot JC, Vignat N, Artigou JY (2010) Cardiac side-effects of cancer chemotherapy. Int J Cardiol 144(1):3–15. doi:10.1016/j.ijcard.2010.03.003

    Article  PubMed  Google Scholar 

  20. Chen B, Peng X, Pentassuglia L, Lim CC, Sawyer DB (2007) Molecular and cellular mechanisms of anthracycline cardiotoxicity. Cardiovasc Toxicol 7(2):114–121

    Article  CAS  PubMed  Google Scholar 

  21. Plana JC, Galderisi M, Barac A et al (2014) Expert consensus for multimodality imaging evaluation of adult patients during and after cancer therapy: a report from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. J Am Soc Echocardiog 27(9):911–939. doi:10.1016/j.echo.2014.07.012

    Article  Google Scholar 

  22. Ewer MS, Ali MK, Mackay B, Wallace S, Valdivieso M, Legha SS, Benjamin RS, Haynie TP (1984) A comparison of cardiac biopsy grades and ejection fraction estimations in patients receiving adriamycin. J Clin Oncol 2(2):112–117

    Article  CAS  PubMed  Google Scholar 

  23. Thavendiranathan P, Poulin F, Lim KD, Plana JC, Woo A, Marwick TH (2014) Use of myocardial strain imaging by echocardiography for the early detection of cardiotoxicity in patients during and after cancer chemotherapy: a systematic review. J Am Coll Cardiol 63(25 Pt A):2751–2768. doi:10.1016/j.jacc.2014.01.073

    Article  PubMed  Google Scholar 

  24. Kang Y, Xu X, Cheng L, Li L, Sun M, Chen H, Pan C, Shu X (2014) Two-dimensional speckle tracking echocardiography combined with high-sensitive cardiac troponin T in early detection and prediction of cardiotoxicity during epirubicine-based chemotherapy. Eur J Heart Fail 16(3):300–308. doi:10.1002/ejhf.8

    Article  CAS  PubMed  Google Scholar 

  25. Mavinkurve-Groothuis AM, Marcus KA, Pourier M, Loonen J, Feuth T, Hoogerbrugge PM, de Korte CL, Kapusta L (2013) Myocardial 2D strain echocardiography and cardiac biomarkers in children during and shortly after anthracycline therapy for acute lymphoblastic leukaemia (ALL): a prospective study. Eur Heart J Cardiovasc Imaging 14(6):562–569. doi:10.1093/ehjci/jes217

    Article  PubMed  Google Scholar 

  26. Luis SA, Yamada A, Khandheria BK, Speranza V, Benjamin A, Ischenko M, Platts DG, Hamilton-Craig CR, Haseler L, Burstow D, Chan J (2014) Use of three-dimensional speckle-tracking echocardiography for quantitative assessment of global left ventricular function: a comparative study to three-dimensional echocardiography. J Am Soc Echocardiogr 27(3):285–291. doi:10.1016/j.echo.2013.11.002

    Article  PubMed  Google Scholar 

  27. Ozawa K, Funabashi N, Takaoka H, Kamata T, Nomura F, Kobayashi Y (2015) Consistencies of 3D TTE global longitudinal strain of both ventricles between assessors were worse for 2D, but better for 3D ventricular EF. Int J Cardiol 198:140–151

    Article  PubMed  Google Scholar 

  28. Castel AL, Menet A, Ennezat PV, Delelis F, Le Goffic C, Binda C, Guerbaai RA, Levy F, Graux P, Tribouilloy C, Maréchaux S (2016) Global longitudinal strain software upgrade: Implications for intervendor consistency and longitudinal imaging studies. Arch Cardiovasc Dis 109(1):22–30

    Article  PubMed  Google Scholar 

  29. Zamorano JL, Lancellotti P, Rodriguez Muñoz D et al (2016) 2016 ESC position paper on cancer treatments and cardiovascular toxicity developed under the auspices of the ESC Committee for Practice Guidelines: the Task Force for cancer treatments and cardiovascular toxicity of the European Society of Cardiology (ESC). Eur J Heart Fail. doi:10.1002/ejhf.654

    Google Scholar 

  30. Mornoş C, Manolis AJ, Cozma D, Kouremenos N, Zacharopoulou I, Ionac A (2014) The value of left ventricular global longitudinal strain assessed by three-dimensional strain imaging in the early detection of anthracycline-mediated cardiotoxicity. Hellenic J Cardiol 55(3):235–244

    PubMed  Google Scholar 

  31. Armstrong GT, Joshi VM, Ness KK, Marwick TH, Zhang N, Srivastava D, Griffin BP, Grimm RA, Thomas J, Phelan D, Collier P, Krull KR, Mulrooney DA, Green DM, Hudson MM, Robison LL, Plana JC (2015) Comprehensive echocardiographic detection of treatment-related cardiac dysfunction in adult survivors of childhood cancer: results From the St. Jude Lifetime Cohort Study. J Am Coll Cardiol 65(23):2511–2522. doi:10.1016/j.jacc.2015.04.013

    Article  PubMed  PubMed Central  Google Scholar 

  32. Takigiku K, Takeuchi M, Izumi C, Yuda S, Sakata K, Ohte N, Tanabe K, Nakatani S, JUSTICE Investigators (2012) Normal range of left ventricular 2-dimensional strain: Japanese Ultrasound Speckle Tracking of the Left Ventricle (JUSTICE) study. Circ J 76(11):2623–2632.

    Article  PubMed  Google Scholar 

  33. Toro-Salazar OH, Ferranti J, Lorenzoni R, Walling S, Mazur W, Raman SV, Davey BT, Gillan E, O’Loughlin M, Klas B, Hor KN (2016) Feasibility of echocardiographic techniques to detect subclinical cancer therapeutics-related cardiac dysfunction among high-dose patients when compared with cardiac magnetic resonance imaging. J Am Soc Echocardiogr 29(2):119–131. doi:10.1016/j.echo.2015.10.008

    Article  PubMed  Google Scholar 

  34. Miyoshi T, Tanaka H, Kaneko A, Tatsumi K, Matsumoto K, Minami H, Kawai H, Hirata K (2014) Left ventricular endocardial dysfunction in patients with preserved ejection fraction after receiving anthracycline. Echocardiography 31(7):848–857. doi:10.1111/echo.12473

    PubMed  Google Scholar 

  35. Milano G, Raucci A, Scopece A, Daniele R, Guerrini U, Sironi L, Cardinale D, Capogrossi MC, Pompilio G (2014) Doxorubicin and trastuzumab regimen induces biventricular failure in mice. J Am Soc Echocardiogr 27(5):568–579. doi:10.1016/j.echo.2014.01.014

    Article  PubMed  Google Scholar 

  36. Bing R, Naoum C, Kritharides L (2015) The vulnerable right ventricle: recurrent, transient right ventricular failure on a background of systemic sclerosis and previous anthracycline exposure. Int J Cardiol 178:223–225. doi:10.1016/j.ijcard.2014.10.078

    Article  PubMed  Google Scholar 

  37. Lu KJ, Chen JX, Profitis K, Kearney LG, DeSilva D, Smith G, Ord M, Harberts S, Calafiore P, Jones E, Srivastava PM (2015) Right ventricular global longitudinal strain is an independent predictor of right ventricular function: a multimodality study of cardiac magnetic resonance imaging, real time three-dimensional echocardiography and speckle tracking echocardiography. Echocardiography 32(6):966–974. doi:10.1111/echo.12783

    Article  PubMed  Google Scholar 

  38. Tanindi A, Demirci U, Tacoy G, Buyukberber S, Alsancak Y, Coskun U, Yalcin R, Benekli M (2011) Assessment of right ventricular functions during cancer chemotherapy. Eur J Echocardiogr 12(11):834–840. doi:10.1093/ejechocard/jer142

    Article  PubMed  Google Scholar 

  39. Grover S, Leong DP, Chakrabarty A, Joerg L, Kotasek D, Cheong K, Joshi R, Joseph MX, DePasquale C, Koczwara B, Selvanayagam JB (2013) Left and right ventricular effects of anthracycline and trastuzumab chemotherapy: a prospective study using novel cardiac imaging and biochemical markers. Int J Cardiol 168(6):5465–5467. doi:10.1016/j.ijcard.2013.07.246

    Article  PubMed  Google Scholar 

  40. Kocabaş A, Kardelen F, Ertuğ H, Aldemir-Kocabaş B, Tosun Ö, Yeşilipek A, Hazar V, Akçurin G (2014) Assessment of early-onset chronic progressive anthracycline cardiotoxicity in children: different response patterns of right and left ventricles. Pediatr Cardiol 35(1):82–88. doi:10.1007/s00246-013-0745-x

    Article  PubMed  Google Scholar 

  41. Anavekar NS, Gerson D, Skali H, Kwong RY, Yucel EK, Solomon SD (2007) Two-dimensional assessment of right ventricular function: an echocardiographic-MRI correlative study. Echocardiography 24(5):452–456

    Article  PubMed  Google Scholar 

  42. Yağci-Küpeli B, Varan A, Yorgun H, Kaya B, Büyükpamukçu M (2012) Tissue doppler and myocardial deformation imaging to detect myocardial dysfunction in pediatric cancer patients treated with high doses of anthracyclines. Asia Pac J Clin Oncol 8(4):368–374. doi:10.1111/j.1743-7563.2012.01566x

    Article  PubMed  Google Scholar 

  43. Bayram C, Çetin İ, Tavil B, Yarali N, Ekici F, Isık P, Tunc B (2015) Evaluation of cardiotoxicity by tissue doppler imaging in childhood leukemia survivors treated with low-dose anthracycline. Pediatr Cardiol 36(4):862–866. doi:10.1007/s00246-015-1096-6

    Article  PubMed  Google Scholar 

  44. Sanchis J, Bardají A, Bosch X, Loma-Osorio P, Marín F, Sánchez PL, Calvo F, Avanzas P, Hernández C, Serrano S, Carratalá A, Barrabés JA (2013) N-terminal pro-brain natriuretic peptide and high-sensitivity troponin in the evaluation of acute chest pain of uncertain etiology. A PITAGORAS substudy. Rev Esp Cardiol (Engl) 66(7):532–538. doi:10.1016/j.rec.2012.11.004

    Article  Google Scholar 

  45. Blaes AH, Rehman A, Vock DM, Luo X, Menge M, Yee D, Missov E, Duprez D (2015) Utility of high-sensitivity cardiac troponin T in patients receiving anthracycline chemotherapy. Vasc Health Risk Manag 11:591–594. doi:10.2147/VHRM.S89842

    Article  PubMed  PubMed Central  Google Scholar 

  46. Zidan A, Sherief LM, El-sheikh A, Saleh SH, Shahbah DA, Kamal NM, Sherbiny HS, Ahmad H (2015) NT-proBNP as early marker of subclinical late cardiotoxicity after doxorubicin therapy and mediastinal irradiation in childhood cancer survivors. Dis Markers 2015:513219. doi:10.1155/2015/513219

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by programs from the National Nature Science Foundation of China (81201095) and the Excellence Award for Youth Talent of Zhongshan Hospital, Fudan University (2015ZSYXGG04).

Authors’ contributions

LC and YG designed the study, FS and JS carried the study, FS, CZ, YX and QZ analyzed the study’s data, FS, JS and XS wrote the manuscript, LC and YG corrected the manuscript. All authors approved the final version of the manuscript.

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Correspondence to Ye Guo or Lei-Lei Cheng.

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All authors declare that they have no conflict of interest.

Ethical approval

All subjects provided informed consent for participation in the study and for the administration of anthracycline therapy. The local ethics committee approved the protocol (the ethics approval number of Fudan University Shanghai Cancer Center is: 1212117-6, the ethics approval number of Zhongshan Hospital of Fudan University is: 2011-117).

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Fei-Yan Song and Jing Shi have contributed equally.

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Song, FY., Shi, J., Guo, Y. et al. Assessment of biventricular systolic strain derived from the two-dimensional and three-dimensional speckle tracking echocardiography in lymphoma patients after anthracycline therapy. Int J Cardiovasc Imaging 33, 857–868 (2017). https://doi.org/10.1007/s10554-017-1082-6

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