Understanding cardiovascular injury after treatment for cancer: an overview of current uses and future directions of cardiovascular magnetic resonance

Journal of Cardiovascular Magnetic Resonance

W Gregory Hundley¹  Sujethra Vasu² 

[1] DepartmentRadiology, Wake Forest School of Medicine, Winston-Salem, North Carolina, USA;Department of Internal Medicine (Section on Cardiology), Wake Forest School of Medicine, Winston-Salem, North Carolina, USA

关键词: Cardiovascular magnetic resonance;    Cancer;    Chemotherapy;    Cardiotoxicity;   

Others  :  812413
DOI  :  10.1186/1532-429X-15-66

 received in 2013-04-12, accepted in 2013-07-07,  发布年份 2013

【 摘 要 】

While cancer-free survival has improved over the past 20 years for many individuals with prostate, renal, breast, and hematologic malignancies, the increasingly recognized prevalence of cardiovascular (CV) events in cancer survivors has been an unintended consequence of many of the therapies that have improved these survival rates. The increase in CV events threatens to offset the improvement in cancer related survival. As a result, there is an emerging need to develop methods to identify those individuals treated for cancer at increased risk of cardiovascular events. With its inherent ability to characterize myocardial tissue and identify both cardiac and vascular dysfunction, cardiovascular magnetic resonance (CMR) has the potential to identify both subclinical and early clinical CV injury before the development of an overt catastrophic event such as a myocardial infarction, stroke, or premature cardiac death. Early identification provides an opportunity for the implementation of primary prevention strategies to prevent such events, thereby improving overall cancer survivorship and quality of life. This article reviews the etiology of CV events associated with cancer therapy and the unique potential of CMR to provide early diagnosis of subclinical CV injury related to the administration of these therapies.

【 授权许可】

   
2013 Vasu and Hundley; licensee BioMed Central Ltd.

【 图 表 】

Figure 2.

Figure 3.

Figure 4.

Figure 5.

【 参考文献 】

• [1]Bowles EJ, Wellman R, Feigelson HS, Onitilo AA, Freedman AN, Delate T, Allen LA, Nekhlyudov L, Goddard KA, Davis RL et al.. Risk of heart failure in breast cancer patients after anthracycline and trastuzumab treatment: a retrospective cohort study. J Natl Cancer Inst. 2012; 104:1293-305.
• [2]Brenner H. Long-term survival rates of cancer patients achieved by the end of the 20th century: a period analysis. Lancet. 2002; 360:1131-5.
• [3]Coughlin SS, Ekwueme DU. Breast cancer as a global health concern. Cancer Epidemiol. 2009; 33:315-8.
• [4]Du XL, Fox EE, Lai D. Competing causes of death for women with breast cancer and change over time from 1975 to 2003. Am J Clin Oncol. 2008; 31:105-16.
• [5]Geiger AM. Trastuzumab and congestive heart failure: what can we learn from use in the community? J Natl Cancer Inst. 2012; 104:1269-70.
• [6]Hooning MJ, Botma A, Aleman BM, Baaijens MH, Bartelink H, Klijn JG, Taylor CW, van Leeuwen FE. Long-term risk of cardiovascular disease in 10-year survivors of breast cancer. J Natl Cancer Inst. 2007; 99:365-75.
• [7]Maurea N, Coppola C, Ragone G, Frasci G, Bonelli A, Romano C, Iaffaioli RV. Women survive breast cancer but fall victim to heart failure: the shadows and lights of targeted therapy. J Cardiovasc Med (Hagerstown). 2010; 11:861-8.
• [8]Patnaik JL, Byers T, DiGuiseppi C, Dabelea D, Denberg TD. Cardiovascular disease competes with breast cancer as the leading cause of death for older females diagnosed with breast cancer: a retrospective cohort study. Breast Cancer Res. 2011; 13:R64. BioMed Central Full Text
• [9]Pinder MC, Duan Z, Goodwin JS, Hortobagyi GN, Giordano SH. Congestive heart failure in older women treated with adjuvant anthracycline chemotherapy for breast cancer. J Clin Oncol. 2007; 25:3808-15.
• [10]Schultz PN, Beck ML, Stava C, Vassilopoulou-Sellin R. Health profiles in 5836 long-term cancer survivors. Int J Cancer. 2003; 104:488-95.
• [11]Sukel MP, Breekveldt-Postma NS, Erkens JA, van der Linden PD, Beiderbeck AB, Coebergh JW, Herings RM. Incidence of cardiovascular events in breast cancer patients receiving chemotherapy in clinical practice. Pharmacoepidemiol Drug Saf. 2008; 17:125-34.
• [12]Yood MU, Wells KE, Alford SH, Dakki H, Beiderbeck AB, Hurria A, Gross CP, Oliveria SA. Cardiovascular outcomes in women with advanced breast cancer exposed to chemotherapy. Pharmacoepidemiol Drug Saf. 2012; 21:818-27.
• [13]SEER Cancer Statistics Review, 1975–2008. http://seer. cancer.gov/csr/1975_2008/ webcite, based on November 2010 SEER data submission, posted to the SEER web site, 2011
• [14]Cancer Facts & Figures 2012. http://www. cancer.org/acs/groups/content/@epidemiologysurveilance/documents/document/acspc-031941.pdf webcite
• [15]Smith LA, Cornelius VR, Plummer CJ, Levitt G, Verrill M, Canney P, Jones A. Cardiotoxicity of anthracycline agents for the treatment of cancer: systematic review and meta-analysis of randomised controlled trials. BMC Cancer. 2010; 10:337. BioMed Central Full Text
• [16]Seidman A, Hudis C, Pierri MK, Shak S, Paton V, Ashby M, Murphy M, Stewart SJ, Keefe D. Cardiac dysfunction in the trastuzumab clinical trials experience. J Clin Oncol. 2002; 20:1215-21.
• [17]Keating NL, O’Malley AJ, Smith MR. Diabetes and cardiovascular disease during androgen deprivation therapy for prostate cancer. J Clin Oncol. 2006; 24(27):4448-56.
• [18]Pugh TJ, Ballonoff A, Rusthoven KE, McCammon R, Kavanagh B, Newman F, Rabinovitch R. Cardiac mortality in patients with stage I and II diffuse large B-cell lymphoma treated with and without radiation: a surveillance, epidemiology, and end-results analysis. Int J Radiat Oncol Biol Phys. 2010; 76:845-9.
• [19]Darby SC, Ewertz M, McGale P, Bennet AM, Blom-Goldman U, Brønnum D, Correa C, Cutter D, Gagliardi G, Gigante B et al.. Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med. 2013; 368:987-998.
• [20]Meacham LR, Chow EJ, Ness KK, Kamdar KY, Chen Y, Yasui Y, Oeffinger KC, Sklar CA, Robison LL, Mertens AC. Cardiovascular risk factors in adult survivors of pediatric cancer–a report from the childhood cancer survivor study. Cancer Epidemiol Biomarkers Prev. 2010; 19:170-81.
• [21]Doyle JJ, Neugut AI, Jacobson JS, Grann VR, Hershman DL. Chemotherapy and cardiotoxicity in older breast cancer patients: a population-based study. J Clin Oncol. 2005; 23:8597-605.
• [22]Diller L, Chow EJ, Gurney JG, Hudson MM, Kadin-Lottick NS, Kawashima TI, Leisenring WM, Meacham LR, Mertens AC, Mulrooney DA et al.. Chronic disease in the childhood cancer survivor study cohort: a review of published findings. J Clin Oncol. 2009; 27:2339-55.
• [23]Guarneri V, Lenihan DJ, Valero V, Durand JB, Broglio K, Hess KR, Michaud LB, Gonzalez-Angulo AM, Hortobagyi GN, Esteva FJ. Long-term cardiac tolerability of trastuzumab in metastatic breast cancer: the M.D. Anderson Cancer Center experience. J Clin Oncol. 2006; 24:4107-15.
• [24]Mulrooney DA, Yeazel MW, Kawashima T, Mertens AC, Mitby P, Stovall M, Donaldson SS, Green DM, Sklar CA, Robison LL, Leisenring WM. Cardiac outcomes in a cohort of adult survivors of childhood and adolescent cancer: retrospective analysis of the Childhood Cancer Survivor Study cohort. BMJ. 2009; 339:b4606.
• [25]Perez EA, Rodeheffer R. Clinical cardiac tolerability of trastuzumab. J Clin Oncol. 2004; 22:322-9.
• [26]Steinberger J, Sinaiko AR, Kelly AS, Leisenring WM, Steffen LM, Goodman P, Mulrooney DA, Dietz AC, Moran A, Perkins JL, Baker KS. Cardiovascular risk and insulin resistance in childhood cancer survivors. J Pediatr. 2011; 160:494-9.
• [27]Swerdlow AJ, Higgins CD, Smith P, Cunningham D, Hancock BW, Horwich A, Hoskin PJ, Lister A, Radford JA, Rohatiner AZ, Linch DC. Myocardial infarction mortality risk after treatment for Hodgkin disease: a collaborative British cohort study. J Natl Cancer Inst. 2007; 99:206-14.
• [28]Ng AK, Bernardo MP, Weller E, Backstrand KH, Silver B, Marcus KC, Tarbell NJ, Friedberg J, Canellos GP, Mauch PM. Long-term survival and competing causes of death in patients with early-stage Hodgkin’s disease treated at age 50 or younger. J Clin Oncol. 2002; 20:2101-8.
• [29]Bouchardy C, Rapiti E, Usel M, Majno SB, Vlastos G, Benhamou S, Miralbell R, Neyroud-Caspar I, Verkooijen HM, Vinh-Hung V. Excess of cardiovascular mortality among node-negative breast cancer patients irradiated for inner-quadrant tumors. Ann Oncol. 2010; 21:459-65.
• [30]Bouillon K, Haddy N, Delaloge S, Garbay JR, Garsi JP, Brindel P, Mousannif A, Lê MG, Labbe M, Arriagada R et al.. Long-term cardiovascular mortality after radiotherapy for breast cancer. J Am Coll Cardiol. 2011; 57:445-52.
• [31]Curigliano G, Mayer EL, Burstein HJ, Winer EP, Goldhirsch A. Cardiac toxicity from systemic cancer therapy: a comprehensive review. Prog Cardiovasc Dis. 2010; 53:94-104.
• [32]Roychoudhuri R, Robinson D, Putcha V, Cuzick J, Darby S, Møller H. Increased cardiovascular mortality more than fifteen years after radiotherapy for breast cancer: a population-based study. BMC Cancer. 2007; 7:9. BioMed Central Full Text
• [33]Yeh ET, Bickford CL. Cardiovascular complications of cancer therapy: incidence, pathogenesis, diagnosis, and management. J Am Coll Cardiol. 2009; 53:2231-47.
• [34]Crone SA, Zhao YY, Fan L, Gu Y, Minamisawa S, Liu Y, Peterson KL, Chen J, Kahn R, Condorelli G et al.. ErbB2 is essential in the prevention of dilated cardiomyopathy. Nat Med. 2002; 8:459-65.
• [35]Slamon DJ, Leyland-Jones B, Shak S, Fuchs H, Paton V, Bajamonde A, Fleming T, Eiermann W, Wolter J, Pegram M et al.. Use of chemotherapy plus a monoclonal antibody against HER2 for metastatic breast cancer that overexpresses HER2. N Engl J Med. 2001; 344:783-92.
• [36]Slamon D, Eiermann W, Robert N, Pienkowski T, Martin M, Press M, Mackey J, Glaspy J, Chan A, Pawlicki M et al.. Adjuvant trastuzumab in HER2-positive breast cancer. N Engl J Med. 2011; 365:1273-83.
• [37]Piccart-Gebhart MJ, Procter M, Leyland-Jones B, Goldhirsch A, Untch M, Smith I, Gianni L, Baselga J, Bell R, Jackisch C et al.. Trastuzumab after adjuvant chemotherapy in HER2-positive breast cancer. N Engl J Med. 2005; 353:1659-72.
• [38]Tan-Chiu E, Yothers G, Romond E, Geyer CE, Ewer M, Keefe D, Shannon RP, Swain SM, Brown A, Fehrenbacher L et al.. Assessment of cardiac dysfunction in a randomized trial comparing doxorubicin and cyclophosphamide followed by paclitaxel, with or without trastuzumab as adjuvant therapy in node-positive, human epidermal growth factor receptor 2-overexpressing breast cancer: NSABP B-31. J Clin Oncol. 2005; 23:7811-9.
• [39]Amir E, Seruga B, Niraula S, Carlsson L, Ocaña A. Toxicity of adjuvant endocrine therapy in postmenopausal breast cancer patients: a systematic review and meta-analysis. J Natl Cancer Inst. 2011; 103:1299-309.
• [40]Goss PE, Ingle JN, Martino S, Robert NJ, Muss HB, Piccart MJ, Castiglione M, Tu D, Shepherd LE, Pritchard KI et al.. A randomized trial of letrozole in postmenopausal women after five years of tamoxifen therapy for early-stage breast cancer. N Engl J Med. 2003; 349:1793-802.
• [41]Huggins C, Hodges CV. Studies on prostatic cancer: I. The effect of castration, of estrogen and of androgen injection on serum phosphatases in metastatic carcinoma of the prostate. 1941. J Urol. 2002; 168:9-12.
• [42]Thurlimann B, Keshaviah A, Coates AS, Mouridsen H, Mauriac L, Forbes JF, Paridaens R, Castiglione-Gertsch M, Gelber RD, Rabaglio M et al.. A comparison of letrozole and tamoxifen in postmenopausal women with early breast cancer. N Engl J Med. 2005; 353:2747-57.
• [43]Chapman JA, Meng D, Shepherd L, Parulekar W, Ingle JN, Muss HB, Palmer M, Yu C, Goss PE. Competing causes of death from a randomized trial of extended adjuvant endocrine therapy for breast cancer. J Natl Cancer Inst. 2008; 100:252-60.
• [44]Ewer MS, Gluck S. A woman’s heart: the impact of adjuvant endocrine therapy on cardiovascular health. Cancer. 2009; 115:1813-26.
• [45]Hu JC, Williams SB, O’Malley AJ, Smith MR, Nguyen PL, Keating NL. Androgen-deprivation therapy for nonmetastatic prostate cancer is associated with an increased risk of peripheral arterial disease and venous thromboembolism. Eur Urol. 2012. .
• [46]Keating NL, O’Malley AJ, Freedland SJ, Smith MR. Diabetes and cardiovascular disease during androgen deprivation therapy: observational study of veterans with prostate cancer. J Natl Cancer Inst. 2010; 102:39-46.
• [47]Van Hemelrijck M, Garmo H, Holmberg L, Ingelsson E, Bratt O, Bill-Axelson A, Lambe M, Stattin P, Adolfsson J. Absolute and relative risk of cardiovascular disease in men with prostate cancer: results from the Population-Based PCBaSe Sweden. J Clin Oncol. 2010; 28:3448-56.
• [48]Azoulay L, Yin H, Benayoun S, Renoux C, Boivin JF, Suissa S. Androgen-deprivation therapy and the risk of stroke in patients with prostate cancer. Eur Urol. 2011; 60:1244-50.
• [49]Buzdar A, Howell A, Cuzick J, Wale C, Distler W, Hoctin-Boes G, Houghton J, Locker GY, Nabholtz JM. Comprehensive side-effect profile of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: long-term safety analysis of the ATAC trial. Lancet Oncol. 2006; 7:633-43.
• [50]Meinardi MT, van der Graaf WT, van Veldhuisen DJ, Gietema JA, de Vries EG, Sleijfer DT. Detection of anthracycline-induced cardiotoxicity. Cancer Treat Rev. 1999; 25:237-47.
• [51]Billingham ME, Mason JW, Bristow MR, Daniels JR. Anthracycline cardiomyopathy monitored by morphologic changes. Cancer Treat Rep. 1978; 62:865-72.
• [52]Isner JM, Ferrans VJ, Cohen SR, Witkind BG, Virmani R, Gottdiener JS, Beck JR, Roberts WC. Clinical and morphologic cardiac findings after anthracycline chemotherapy. Analysis of 64 patients studied at necropsy. Am J Cardiol. 1983; 51:1167-74.
• [53]Alexander J, Dainiak N, Berger HJ, Goldman L, Johnstone D, Reduto L, Duffy T, Schwartz P, Gottschalk A, Zaret BL. Serial assessment of doxorubicin cardiotoxicity with quantitative radionuclide angiocardiography. N Engl J Med. 1979; 300:278-83.
• [54]McKillop JH, Bristow MR, Goris ML, Billingham ME, Bockemuehl K. Sensitivity and specificity of radionuclide ejection fractions in doxorubicin cardiotoxicity. Am Heart J. 1983; 106:1048-56.
• [55]Gottdiener JS, Mathisen DJ, Borer JS, Bonow RO, Myers CE, Barr LH, Schwartz DE, Bacharach SL, Green MV, Rosenberg SA. Doxorubicin cardiotoxicity: assessment of late left ventricular dysfunction by radionuclide cineangiography. Ann Intern Med. 1981; 94:430-5.
• [56]Shankar SM, Marina N, Hudson MM, Hodgson DC, Adams MJ, Landier W, Bhatia S, Meeske K, Chen MH, Kinahan KE et al.. Monitoring for cardiovascular disease in survivors of childhood cancer: report from the cardiovascular disease task force of the children’s oncology group. Pediatrics. 2008; 121:e387-96.
• [57]Steinherz LJ, Graham T, Hurwitz R, Sondheimer HM, Schwartz RG, Shaffer EM, Sandor G, Benson L, Williams R. Guidelines for cardiac monitoring of children during and after anthracycline therapy: report of the cardiology committee of the childrens cancer study group. Pediatrics. 1992; 89:942-9.
• [58]Bittner V, Reeves RC, Digerness SB, Caulfield JB, Pohost GM. 31P NMR spectroscopy in chronic adriamycin cardiotoxicity. Magn Reson Med. 1991; 17:69-81.
• [59]Cardinale D, Lamantia G, Cipolla CM. Troponin I and cardiovascular risk stratification in patients with testicular cancer. J Clin Oncol. 2006; 24:3508-9.
• [60]Cardinale D, Salvatici M, Sandri MT. Review: role of biomarkers in cardioncology. Clin Chem Lab Med. 2011; 49:1937-48.
• [61]Cardinale D, Colombo A, Cipolla CM. Prevention and treatment of cardiomyopathy and heart failure in patients receiving cancer chemotherapy. Curr Treat Options Cardiovasc Med. 2008; 10:486-95.
• [62]Cardinale D, Colombo A, Sandri MT, Lamantia G, Colombo N, Civelli M, Martinelli G, Veglia F, Fiorentini C, Cipolla CM. Prevention of high-dose chemotherapy-induced cardiotoxicity in high-risk patients by angiotensin-converting enzyme inhibition. Circulation. 2006; 114:2474-81.
• [63]Hendel RC, Patel MR, Kramer CM, Poon M, Carr JC, Gerstad NA, Gillam LD, Hodgson JM, Kim RJ, Lesser JR et al.. ACCF/ACR/SCCT/SCMR/ASNC/NASCI/SCAI/SIR 2006 appropriateness criteria for cardiac computed tomography and cardiac magnetic resonance imaging: a report of the American College of Cardiology Foundation Quality Strategic Directions Committee Appropriateness Criteria Working Group, American College of Radiology, Society of Cardiovascular Computed Tomography, Society for Cardiovascular Magnetic Resonance, American Society of Nuclear Cardiology, North American Society for Cardiac Imaging, Society for Cardiovascular Angiography and Interventions, and Society of Interventional Radiology. J Am Coll Cardiol. 2006; 48:1475-97.
• [64]Chaosuwannakit N, D’Agostino R, Hamilton CA, Lane KS, Ntim WO, Lawrence J, Melin SA, Ellis LR, Torti FM, Little WC, Hundley WG. Aortic stiffness increases upon receipt of anthracycline chemotherapy. J Clin Oncol. 2010; 28:166-72.
• [65]Pennell DJ, Sechtem UP, Higgins CB, Manning WJ, Pohost GM, Rademakers FE, van Rossum AC, Shaw LJ, Yucel EK. Clinical indications for cardiovascular magnetic resonance (CMR): Consensus Panel report. J Cardiovasc Magn Reson. 2004; 6:727-65.
• [66]Fallah-Rad N, Walker JR, Wassef A, Lytwyn M, Bohonis S, Fang T, Tian G, Kirkpatrick ID, Singal PK, Krahn M et al.. The utility of cardiac biomarkers, tissue velocity and strain imaging, and cardiac magnetic resonance imaging in predicting early left ventricular dysfunction in patients with human epidermal growth factor receptor II-positive breast cancer treated with adjuvant trastuzumab therapy. J Am Coll Cardiol. 2011; 57:2263-70.
• [67]Banchs J, Jefferies JL, Plana JC, Hundley WG. Imaging for cardiotoxicity in cancer patients. Tex Heart Inst J. 2011; 38:268-9.
• [68]Adams MJ, Hardenbergh PH, Constine LS, Lipshultz SE. Radiation-associated cardiovascular disease. Crit Rev Oncol Hematol. 2003; 45:55-75.
• [69]Schellong G, Riepenhausen M, Bruch C, Kotthoff S, Vogt J, Bolling T, Dieckmann K, Potter R, Heinecke A, Bramswig J, Dorffel W. Late valvular and other cardiac diseases after different doses of mediastinal radiotherapy for Hodgkin disease in children and adolescents: report from the longitudinal GPOH follow-up project of the German-Austrian DAL-HD studies. Pediatr Blood Cancer. 2010; 55:1145-52.
• [70]Galper SL, Yu JB, Mauch PM, Strasser JF, Silver B, Lacasce A, Marcus KJ, Stevenson MA, Chen MH, Ng AK. Clinically significant cardiac disease in patients with Hodgkin lymphoma treated with mediastinal irradiation. Blood. 2011; 117:412-8.
• [71]Chiles C, Woodard PK, Gutierrez FR, Link KM. Metastatic involvement of the heart and pericardium: CT and MR imaging. Radiographics. 2001; 21:439-49.
• [72]Abraham KP, Reddy V, Gattuso P. Neoplasms metastatic to the heart: review of 3314 consecutive autopsies. Am J Cardiovasc Pathol. 1990; 3:195-8.
• [73]Mason JW, Bristow MR, Billingham ME, Daniels JR. Invasive and noninvasive methods of assessing adriamycin cardiotoxic effects in man: superiority of histopathologic assessment using endomyocardial biopsy. Cancer Treat Rep. 1978; 62:857-64.
• [74]Thompson RC, Canby RC, Lojeski EW, Ratner AV, Fallon JT, Pohost GM. Adriamycin cardiotoxicity and proton nuclear magnetic resonance relaxation properties. Am Heart J. 1987; 113:1444-9.
• [75]Cottin Y, Ribuot C, Maupoil V, Godin D, Arnould L, Brunotte F, Rochette L. Early incidence of adriamycin treatment on cardiac parameters in the rat. Can J Physiol Pharmacol. 1994; 72:140-5.
• [76]Wassmuth R, Lentzsch S, Erdbruegger U, Schulz-Menger J, Doerken B, Dietz R, Friedrich MG. Subclinical cardiotoxic effects of anthracyclines as assessed by magnetic resonance imaging-a pilot study. Am Heart J. 2001; 141:1007-13.
• [77]Lightfoot JC, D’Agostino RB, Hamilton CA, Jordan J, Torti FM, Kock ND, Workman S, Hundley WG. Novel approach to early detection of doxorubicin cardiotoxicity by gadolinium-enhanced cardiovascular magnetic resonance imaging in an experimental model. Circ Cardiovasc Imaging. 2010; 3:550-8.
• [78]Broberg CS, Chugh SS, Conklin C, Sahn DJ, Jerosch-Herold M. Quantification of diffuse myocardial fibrosis and its association with myocardial dysfunction in congenital heart disease. Circ Cardiovasc Imaging. 2010; 3:727-34.
• [79]Jerosch-Herold M, Sheridan DC, Kushner JD, Nauman D, Burgess D, Dutton D, Alharethi R, Li D, Hershberger RE. Cardiac magnetic resonance imaging of myocardial contrast uptake and blood flow in patients affected with idiopathic or familial dilated cardiomyopathy. Am J Physiol Heart Circ Physiol. 2008; 295:H1234-42.
• [80]Schelbert EB, Testa SM, Meier CG, Ceyrolles WJ, Levenson JE, Blair AJ, Kellman P, Jones BL, Ludwig DR, Schwartzman D et al.. Myocardial extravascular extracellular volume fraction measurement by gadolinium cardiovascular magnetic resonance in humans: slow infusion versus bolus. J Cardiovasc Magn Reson. 2011; 13:16. BioMed Central Full Text
• [81]Messroghli DR, Greiser A, Fröhlich M, Dietz R, Schulz-Menger J. Optimization and validation of a fully-integrated pulse sequence for modified look-locker inversion-recovery (MOLLI) T1 mapping of the heart. J Magn Reson Imaging. 2007; 26:1081-6.
• [82]Messroghli DR, Plein S, Higgins DM, Walters K, Jones TR, Ridgway JP, Sivananthan MU. Human myocardium: single-breath-hold MR T1 mapping with high spatial resolution–reproducibility study. Radiology. 2006; 238:1004-12.
• [83]Messroghli DR, Radjenovic A, Kozerke S, Higgins DM, Sivananthan MU, Ridgway JP. Modified Look-Locker inversion recovery (MOLLI) for high-resolution T1 mapping of the heart. Magn Reson Med. 2004; 52:141-6.
• [84]Flett AS, Hayward MP, Ashworth MT, Hansen MS, Taylor AM, Elliott PM, McGregor C, Moon JC. Equilibrium contrast cardiovascular magnetic resonance for the measurement of diffuse myocardial fibrosis: preliminary validation in humans. Circulation. 2010; 122:138-44.
• [85]Wong TC, Piehler K, Puntil KS, Moguillansky D, Meier CG, Lacomis JM, Kellman P, Cook SC, Schwartzman DS, Simon MA et al.. Effectiveness of late gadolinium enhancement to improve outcomes prediction in patients referred for cardiovascular magnetic resonance after echocardiography. J Cardiovasc Magn Reson. 2013; 15:6. BioMed Central Full Text
• [86]Schwartz RG, McKenzie WB, Alexander J, Sager P, D’Souza A, Manatunga A, Schwartz PE, Berger HJ, Setaro J, Surkin L et al.. Congestive heart failure and left ventricular dysfunction complicating doxorubicin therapy. Seven-year experience using serial radionuclide angiocardiography. Am J Med. 1987; 82:1109-18.
• [87]Jones AL, Barlow M, Barrett-Lee PJ, Canney PA, Gilmour IM, Robb SD, Plummer CJ, Wardley AM, Verrill MW. Management of cardiac health in trastuzumab-treated patients with breast cancer: updated United Kingdom National Cancer Research Institute recommendations for monitoring. Br J Cancer. 2009; 100:684-92.
• [88]Bovelli D, Plataniotis G, Roila F. Cardiotoxicity of chemotherapeutic agents and radiotherapy-related heart disease: ESMO Clinical Practice Guidelines. Ann Oncol. 2010; 21 Suppl 5:v277-82.
• [89]Grothues F, Smith GC, Moon JC, Bellenger NG, Collins P, Klein HU, Pennell DJ. Comparison of interstudy reproducibility of cardiovascular magnetic resonance with two-dimensional echocardiography in normal subjects and in patients with heart failure or left ventricular hypertrophy. Am J Cardiol. 2002; 90:29-34.
• [90]Pattynama PM, Lamb HJ, van der Velde EA, van der Wall EE, de Roos A. Left ventricular measurements with cine and spin-echo MR imaging: a study of reproducibility with variance component analysis. Radiology. 1993; 187:261-8.
• [91]Stoodley PW, Richards DA, Hui R, Boyd A, Harnett PR, Meikle SR, Clarke J, Thomas L. Two-dimensional myocardial strain imaging detects changes in left ventricular systolic function immediately after anthracycline chemotherapy. Eur J Echocardiogr. 2011; 12:945-52.
• [92]Motoki H, Borowski AG, Shrestha K, Troughton RW, Tang WH, Thomas JD, Klein AL. Incremental prognostic value of assessing left ventricular myocardial mechanics in patients with chronic systolic heart failure. J Am Coll Cardiol. 2012; 60:2074-81.
• [93]Cho GY, Marwick TH, Kim HS, Kim MK, Hong KS, Oh DJ. Global 2-dimensional strain as a new prognosticator in patients with heart failure. J Am Coll Cardiol. 2009; 54:618-24.
• [94]Bellavia D, Abraham RS, Pellikka PA, Dispenzieri A, Burnett JC, Al-Zahrani GB, Green TD, Manske MK, Gertz MA, Miller FA, Abraham TP. Utility of Doppler myocardial imaging, cardiac biomarkers, and clonal immunoglobulin genes to assess left ventricular performance and stratify risk following peripheral blood stem cell transplantation in patients with systemic light chain amyloidosis (Al). J Am Soc Echocardiogr. 2011; 24:444-54.
• [95]Saito M, Okayama H, Yoshii T, Higashi H, Morioka H, Hiasa G, Sumimoto T, Inaba S, Nishimura K, Inoue K et al.. Clinical significance of global two-dimensional strain as a surrogate parameter of myocardial fibrosis and cardiac events in patients with hypertrophic cardiomyopathy. Eur Heart J Cardiovasc Imaging. 2012; 13:617-23.
• [96]Drafts BC, Twomley KM, D’Agostino RB, Lawrence JA, Avis NE, Ellis LR, Thohan V, Jordan J, Melin SA, Torti FM et al.. Low to moderate dose anthracyline-based chemotherapy is associated with early noninvasive imaging evidence of subclinical cardiovascular disease. JACC Cardiovasc Imaging. 2012. . Accepted for publication
• [97]Pituskin E, Haykowsky M, Mackey JR, Thompson RB, Ezekowitz J, Koshman S, Oudit G, Chow K, Pagano JJ, Paterson I. Rationale and design of the Multidisciplinary Approach to Novel Therapies in Cardiology Oncology Research Trial (MANTICORE 101–Breast): a randomized, placebo-controlled trial to determine if conventional heart failure pharmacotherapy can prevent trastuzumab-mediated left ventricular remodeling among patients with HER2+ early breast cancer using cardiac MRI. BMC Cancer. 2011; 11:318. BioMed Central Full Text
• [98]McGill LA, Ismail TF, Nielles-Vallespin S, Ferreira P, Scott AD, Roughton M, Kilner PJ, Ho SY, McCarthy KP, Gatehouse PD et al.. Reproducibility of in-vivo diffusion tensor cardiovascular magnetic resonance in hypertrophic cardiomyopathy. J Cardiovasc Magn Reson. 2012; 14:86. BioMed Central Full Text
• [99]Rider OJ, Francis JM, Tyler D, Byrne J, Clarke K, Neubauer S. Effects of weight loss on myocardial energetics and diastolic function in obesity. Int J Cardiovasc Imaging. 2013; 29(5):1043-50.
• [100]Saigal CS, Gore JL, Krupski TL, Hanley J, Schonlau M, Litwin MS. Androgen deprivation therapy increases cardiovascular morbidity in men with prostate cancer. Cancer. 2007; 110:1493-500.
• [101]Chu TF, Rupnick MA, Kerkela R, Dallabrida SM, Zurakowski D, Nguyen L, Woulfe K, Pravda E, Cassiola F, Desai J et al.. Cardiotoxicity associated with tyrosine kinase inhibitor sunitinib. Lancet. 2007; 370:2011-9.
• [102]Escudier B, Eisen T, Stadler WM, Szczylik C, Oudard S, Staehler M, Negrier S, Chevreau C, Desai AA, Rolland F et al.. Sorafenib for treatment of renal cell carcinoma: final efficacy and safety results of the phase III treatment approaches in renal cancer global evaluation trial. J Clin Oncol. 2009; 27:3312-8.
• [103]Miller K, Wang M, Gralow J, Dickler M, Cobleigh M, Perez EA, Shenkier T, Cella D, Davidson NE. Paclitaxel plus bevacizumab versus paclitaxel alone for metastatic breast cancer. N Engl J Med. 2007; 357:2666-76.
• [104]Eckman DM, Stacey RB, Rowe R, D. Agostino RJ, Kock ND, Sane DC, Torti FM, Yeboah J, Workman S, Lane KS, Hundley WG. Weekly Doxorubicin increases coronary arteriolar wall and adventitial thickness. PLoS One. 2013; 8:e57554.
• [105]Rerkpattanapipat P, Hundley WG, Link KM, Brubaker PH, Hamilton CA, Darty SN, Morgan TM, Kitzman DW. Relation of aortic distensibility determined by magnetic resonance imaging in patients > or =60 years of age to systolic heart failure and exercise capacity. Am J Cardiol. 2002; 90:1221-5.
• [106]Meeske K, Smith AW, Alfano CM, McGregor BA, McTiernan A, Baumgartner KB, Malone KE, Reeve BB, Ballard-Barbash R, Bernstein L. Fatigue in breast cancer survivors two to five years post diagnosis: a HEAL Study report. Qual Life Res. 2007; 16:947-60.
• [107]Pater JL, Loeb M. Nonanatomic prognostic factors in carcinoma of the lung: a multivariate analysis. Cancer. 1982; 50:326-31.
• [108]Ringdal GI, Gotestam KG, Kaasa S, Kvinnsland S, Ringdal K. Prognostic factors and survival in a heterogeneous sample of cancer patients. Br J Cancer. 1996; 73:1594-9.
• [109]Andersen C, Rørth M, Ejlertsen B, Stage M, Møller T, Midtgaard J, Quist M, Bloomquist K, Adamsen L. The effects of a six-week supervised multimodal exercise intervention during chemotherapy on cancer-related fatigue. Eur J Oncol Nurs. 2013; 17(3):331-9.
• [110]Holmes MD, Chen WY, Feskanich D, Kroenke CH, Colditz GA. Physical activity and survival after breast cancer diagnosis. JAMA. 2005; 293:2479-86.
• [111]Meyerhardt JA, Giovannucci EL, Holmes MD, Chan AT, Chan JA, Colditz GA, Fuchs CS. Physical activity and survival after colorectal cancer diagnosis. J Clin Oncol. 2006; 24:3527-34.
• [112]Hundley WG, Bayram E, Hamilton CA, Hamilton EA, Morgan TM, Darty SN, Stewart KP, Link KM, Herrington DM, Kitzman DW. Leg flow-mediated arterial dilation in elderly patients with heart failure and normal left ventricular ejection fraction. Am J Physiol Heart Circ Physiol. 2007; 292:H1427-34.
• [113]Puntawangkoon C, Kitzman DW, Kritchevsky SB, Hamilton CA, Nicklas B, Leng X, Brubaker PH, Hundley WG. Reduced peripheral arterial blood flow with preserved cardiac output during submaximal bicycle exercise in elderly heart failure. J Cardiovasc Magn Reson. 2009; 11:48. BioMed Central Full Text
• [114]Gilliam LA, Ferreira LF, Bruton JD, Moylan JS, Westerblad H, St Clair DK, Reid MB. Doxorubicin acts through tumor necrosis factor receptor subtype 1 to cause dysfunction of murine skeletal muscle. J Appl Physiol. 2009; 107:1935-42.
• [115]Gilliam LA, Moylan JS, Ann Callahan L, Sumandea MP, Reid MB. Doxorubicin causes diaphragm weakness in murine models of cancer chemotherapy. Muscle Nerve. 2011; 43:94-102.
• [116]Doroshow JH, Tallent C, Schechter JE. Ultrastructural features of Adriamycin-induced skeletal and cardiac muscle toxicity. Am J Pathol. 1985; 118:288-97.
• [117]Jacobi B, Bongartz G, Partovi S, Schulte AC, Aschwanden M, Lumsden AB, Davies MG, Loebe M, Noon GP, Karimi S et al.. Skeletal muscle BOLD MRI: from underlying physiological concepts to its usefulness in clinical conditions. J Magn Reson Imaging. 2012; 35:1253-65.
• [118]Ledermann HP, Heidecker HG, Schulte AC, Thalhammer C, Aschwanden M, Jaeger KA, Scheffler K, Bilecen D. Calf muscles imaged at BOLD MR: correlation with TcPO2 and flowmetry measurements during ischemia and reactive hyperemia–initial experience. Radiology. 2006; 241:477-84.