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Review Article

Fitting the right non-vitamin K antagonist oral anticoagulant to the right patient with non-valvular atrial fibrillation: an evidence-based choice

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Pages 288-302 | Received 02 Feb 2018, Accepted 29 Mar 2018, Published online: 15 Apr 2018

References

  • Wolf PA, Abbott RD, Kannel WB. Atrial fibrillation as an independent risk factor for stroke: the Framingham study. Stroke. 1991;22:983–998.
  • Kimura K, Minematsu K, Yamaguchi T. Japan Multicenter Stroke Investigators C. Atrial fibrillation as a predictive factor for severe stroke and early death in 15,831 patients with acute ischaemic stroke. J Neurol Neurosurg Psychiatry. 2005;76:679–683.
  • Marini C, De Santis F, Sacco S, et al. Contribution of atrial fibrillation to incidence and outcome of ischemic stroke: results from a population-based study. Stroke. 2005;36:1115–1119.
  • Lip GYH. The ABC pathway: an integrated approach to improve AF management. Nat Rev Cardiol. 2017;14:627–628.
  • Lip G, Freedman B, De Caterina R, et al. Stroke prevention in atrial fibrillation: Past, present and future. Comparing the guidelines and practical decision-making. Thromb Haemost. 2017;117:1230–1239.
  • Walraven C, Hart RG, Singer DE, et al. Oral anticoagulants vs aspirin in nonvalvular atrial fibrillation an individual patient meta-analysis. JAMA. 2002;288:2441–2448.
  • Hart RG, Pearce LA, Aguilar MI. Meta-analysis antithrombotic therapy to prevent stroke in patients who have nonvalvular atrial fibrillation. Ann Intern Med. 2007;207:857–867.
  • Connolly SJ, Ezekowitz MD, Ch B, et al. Dabigatran versus warfarin in patients with atrial fibrillation. N Engl J Med. 2009;361:1139–1151.
  • Patel MR, Mahaffey KW, Garg J, et al. Rivaroxaban versus warfarin in nonvalvular atrial fibrillation. N Engl J Med. 2011;365:883–891.
  • Granger CB, Alexander JH, McMurray JJV, et al. Apixaban versus warfarin in patients with atrial fibrillation-ARISTOTLE study. N Engl J Med. 2011;365:981–992.
  • Giugliano RP, Ruff CT, Braunwald E, et al. Edoxaban versus warfarin in patients with atrial fibrillation. N Engl J Med. 2013;369:2093–2104.
  • Hori M, Matsumoto M, Tanahashi N, et al. Rivaroxaban vs. warfarin in Japanese patients with atrial fibrillation. Circ J. 2012;76:2104–2111.
  • Kittelson JM, Steg PG, Halperin JL, et al. Bivariate evaluation of thromboembolism and bleeding in clinical trials of anticoagulants in patients with atrial fibrillation. Thromb Haemost. 2016;116:544–553.
  • Hecker J, Marten S, Keller L, et al. Effectiveness and safety of rivaroxaban therapy in daily-care patients with atrial fibrillation. Results from the Dresden NOAC Registry. Thromb Haemost. 2016;115:939–949.
  • Martinez C, Katholing A, Wallenhorst C, et al. Therapy persistence in newly diagnosed non-valvular atrial fibrillation treated with warfarin or NOAC. A cohort study. Thromb Haemost. 2016;115:31–39.
  • Beyer-Westendorf J, Ebertz F, Forster K, et al. Effectiveness and safety of dabigatran therapy in daily-care patients with atrial fibrillation. Results from the Dresden NOAC Registry. Thromb Haemost. 2015;113:1247–1257.
  • Rivera-Caravaca JM, Roldan V, Esteve-Pastor MA, et al. Cessation of oral anticoagulation is an important risk factor for stroke and mortality in atrial fibrillation patients. Thromb Haemost. 2017;117:1448–1454.
  • Huisman MV, Rothman KJ, Paquette M, et al. The changing landscape for stroke prevention in AF: findings from the GLORIA-AF registry phase 2. J Am Coll Cardiol. 2017;69:777–785.
  • Lip GY, Nieuwlaat R, Pisters R, et al. Refining clinical risk stratification for predicting stroke and thromboembolism in atrial fibrillation using a novel risk factor-based approach: the euro heart survey on atrial fibrillation. Chest. 2010;137:263–272.
  • Rost NS, Giugliano RP, Ruff CT, et al. Outcomes with edoxaban versus warfarin in patients with previous cerebrovascular events: findings from ENGAGE AF-TIMI 48 (effective anticoagulation with factor Xa next generation in atrial fibrillation-thrombolysis in myocardial infarction 48). Stroke. 2016;47:2075–2082.
  • Diener H-C, Eikelboom J, Connolly SJ, et al. Apixaban versus aspirin in patients with atrial fibrillation and previous stroke or transient ischaemic attack: a predefined subgroup analysis from AVERROES, a randomised trial. Lancet Neurol. 2012;11:225–231.
  • Diener H-C, Connolly SJ, Ezekowitz MD, et al. Dabigatran compared with warfarin in patients with atrial fibrillation and previous transient ischaemic attack or stroke: a subgroup analysis of the RE-LY trial. Lancet Neurol. 2010;9:1157–1163.
  • Hankey GJ, Patel MR, Stevens SR, et al. Rivaroxaban compared with warfarin in patients with atrial fibrillation and previous stroke or transient ischaemic attack: a subgroup analysis of ROCKET AF. Lancet Neurol. 2012;11:315–322.
  • Tanahashi N, Hori M, Matsumoto M, et al. Rivaroxaban versus warfarin in Japanese patients with nonvalvular atrial fibrillation for the secondary prevention of stroke: a subgroup analysis of J-ROCKET AF. J Stroke Cerebrovasc Dis. 2013;22:1317–1325.
  • Easton JD, Lopes RD, Bahit MC, et al. Apixaban compared with warfarin in patients with atrial fibrillation and previous stroke or transient ischaemic attack: a subgroup analysis of the ARISTOTLE trial. Lancet Neurol. 2012;11:503–511.
  • Eikelboom JW, Wallentin L, Connolly SJ, et al. Risk of bleeding with 2 doses of dabigatran compared with warfarin in older and younger patients with atrial fibrillation: an analysis of the randomized evaluation of long-term anticoagulant therapy (RE-LY) trial. Circulation. 2011;123:2363–2372.
  • Halperin JL, Hankey GJ, Wojdyla DM, et al. Efficacy and safety of rivaroxaban compared with warfarin among elderly patients with nonvalvular atrial fibrillation in the rivaroxaban once daily, oral, direct factor Xa inhibition compared with vitamin K antagonism for prevention of stroke and embolism trial in atrial fibrillation (ROCKET AF). Circulation. 2014;130:138–146.
  • Ng KH, Shestakovska O, Connolly SJ, et al. Efficacy and safety of apixaban compared with aspirin in the elderly: a subgroup analysis from the AVERROES trial. Age Ageing. 2016;45:77–83.
  • Kato ET, Giugliano RP, Ruff CT, et al. Efficacy and safety of edoxaban in elderly patients with atrial fibrillation in the ENGAGE AF-TIMI 48 trial. J Am Heart Assoc. 2016;5:e003432.
  • Wallentin L, Yusuf S, Ezekowitz MD, et al. Efficacy and safety of dabigatran compared with warfarin at different levels of international normalised ratio control for stroke prevention in atrial fibrillation: an analysis of the RE-LY trial. Lancet. 2010;376:975–983.
  • Piccini JP, Hellkamp AS, Lokhnygina Y, et al. Relationship between time in therapeutic range and comparative treatment effect of rivaroxaban and warfarin: results from the ROCKET AF trial. J Am Heart Assoc. 2014;3:e000521.
  • Wallentin L, Lopes RD, Hanna M, et al. Efficacy and safety of apixaban compared with warfarin at different levels of predicted international normalized ratio control for stroke prevention in atrial fibrillation. Circulation. 2013;127:2166–2176.
  • Hijazi Z, Hohnloser SH, Oldgren J, et al. Efficacy and safety of dabigatran compared with warfarin in relation to baseline renal function in patients with atrial fibrillation: a RE-LY (Randomized Evaluation of Long-term Anticoagulation Therapy) trial analysis. Circulation. 2014;129:961–970.
  • Hori M, Matsumoto M, Tanahashi N, et al. Safety and efficacy of adjusted dose of rivaroxaban in Japanese patients with non-valvular atrial fibrillation. Circ J. 2013;77:632–638.
  • Fox KA, Piccini JP, Wojdyla D, et al. Prevention of stroke and systemic embolism with rivaroxaban compared with warfarin in patients with non-valvular atrial fibrillation and moderate renal impairment. Eur Heart J. 2011;32:2387–2394.
  • Hohnloser SH, Hijazi Z, Thomas L, et al. Efficacy of apixaban when compared with warfarin in relation to renal function in patients with atrial fibrillation: insights from the ARISTOTLE trial. Eur Heart J. 2012;33:2821–2830.
  • Eikelboom JW, Connolly SJ, Gao P, et al. Stroke risk and efficacy of apixaban in atrial fibrillation patients with moderate chronic kidney disease. J Stroke Cerebrovasc Dis. 2012;21:429–435.
  • Mahaffey KW, Stevens SR, White HD, et al. Ischaemic cardiac outcomes in patients with atrial fibrillation treated with vitamin K antagonism or factor Xa inhibition: results from the ROCKET AF trial. Eur Heart J. 2014;35:233–241.
  • Bahit MC, Lopes RD, Wojdyla DM, et al. Apixaban in patients with atrial fibrillation and prior coronary artery disease: insights from the ARISTOTLE trial. Int J Cardiol. 2013;170:215–220.
  • Dans AL, Connolly SJ, Wallentin L, et al. Concomitant use of antiplatelet therapy with dabigatran or warfarin in the randomized evaluation of long-term anticoagulation therapy (RE-LY) trial. Circulation. 2013;127:634–640.
  • Xu H, Ruff CT, Giugliano RP, et al. Concomitant use of single antiplatelet therapy with edoxaban or warfarin in patients with atrial fibrillation: analysis from the ENGAGE AF-TIMI48 trial. J Am Heart Assoc. 2016;5:e002587.
  • Cannon CP, Bhatt DL, Oldgren J, et al. Dual antithrombotic therapy with dabigatran after PCI in atrial fibrillation. N Engl J Med. 2017;377:1513–1524.
  • Gibson CM, Mehran R, Bode C, et al. Prevention of bleeding in patients with atrial fibrillation undergoing PCI. N Engl J Med. 2016;375:2423–2434.
  • Nagarakanti R, Ezekowitz MD, Oldgren J, et al. Dabigatran versus warfarin in patients with atrial fibrillation: an analysis of patients undergoing cardioversion. Circulation. 2011;123:131–136.
  • Piccini JP, Stevens SR, Lokhnygina Y, et al. Outcomes after cardioversion and atrial fibrillation ablation in patients treated with rivaroxaban and warfarin in the ROCKET AF trial. J Am Coll Cardiol. 2013;61:1998–2006.
  • Cappato R, Ezekowitz MD, Klein AL, et al. Rivaroxaban vs. vitamin K antagonists for cardioversion in atrial fibrillation. Eur Heart J. 2014;35:3346–3355.
  • Goette A, Merino JL, Ezekowitz MD, et al. Edoxaban versus enoxaparin–warfarin in patients undergoing cardioversion of atrial fibrillation (ENSURE-AF): a randomised, open-label, phase 3b trial. Lancet. 2016;388:1995–2003.
  • Hori M, Connolly SJ, Zhu J, et al. Dabigatran versus warfarin: effects on ischemic and hemorrhagic strokes and bleeding in Asians and non-Asians with atrial fibrillation. Stroke. 2013;44:1891–1896.
  • Wong KS, Hu DY, Oomman A, et al. Rivaroxaban for stroke prevention in East Asian patients from the ROCKET AF trial. Stroke. 2014;45:1739–1747.
  • Goto S, Zhu J, Liu L, et al. Efficacy and safety of apixaban compared with warfarin for stroke prevention in patients with atrial fibrillation from East Asia: a subanalysis of the apixaban for reduction in stroke and other thromboembolic events in atrial fibrillation (ARISTOTLE) trial. Am Heart J. 2014;168:303–309.
  • Yamashita T, Koretsune Y, Yang Y, et al. Edoxaban vs. warfarin in east Asian patients with atrial fibrillation – an ENGAGE AF-TIMI 48 subanalysis. Circ J. 2016;80:860–869.
  • Sardar P, Chatterjee S, Wu WC, et al. New oral anticoagulants are not superior to warfarin in secondary prevention of stroke or transient ischemic attacks, but lower the risk of intracranial bleeding: insights from a meta-analysis and indirect treatment comparisons. PLoS One. 2013;8:e77694.
  • Katsanos AH, Mavridis D, Parissis J, et al. Novel oral anticoagulants for the secondary prevention of cerebral ischemia: a network meta-analysis. Ther Adv Neurol Disord. 2016;9:359–368.
  • Paciaroni M, Agnelli G, Ageno W, et al. Timing of anticoagulation therapy in patients with acute ischaemic stroke and atrial fibrillation. Thromb Haemost. 2016;116:410–416.
  • Toyoda K, Arihiro S, Todo K, et al. Trends in oral anticoagulant choice for acute stroke patients with nonvalvular atrial fibrillation in Japan: the SAMURAI-NVAF study. Int J Stroke. 2015;10:836–842.
  • Avgil-Tsadok M, Jackevicius CA, Essebag V, et al. Dabigatran use in elderly patients with atrial fibrillation. Thromb Haemost. 2016;115:152–160.
  • Okumura K, Lip GYH, Akao M, et al. Edoxaban for the management of elderly Japanese patients with atrial fibrillation ineligible for standard oral anticoagulant therapies: Rationale and design of the ELDERCARE-AF study. Am Heart J. 2017;194:99–106.
  • White HD, Gruber M, Feyzi J, et al. Comparison of outcomes among patients randomized to warfarin therapy according to anticoagulant control: results from SPORTIF III and V. Arch Intern Med. 2007;167:239–245.
  • Gallego P, Roldan V, Marin F, et al. Cessation of oral anticoagulation in relation to mortality and the risk of thrombotic events in patients with atrial fibrillation. Thromb Haemost. 2013;110:1189–1198.
  • Pastori D, Pignatelli P, Saliola M, et al. Inadequate anticoagulation by Vitamin K Antagonists is associated with major adverse cardiovascular events in patients with atrial fibrillation. Int J Cardiol. 2015;201:513–516.
  • Sjogren V, Bystrom B, Renlund H, et al. Non-vitamin K oral anticoagulants are non-inferior for stroke prevention but cause fewer major bleedings than well-managed warfarin: a retrospective register study. PLoS One. 2017;12:e0181000.
  • Piccini JP, Stevens SR, Chang Y, et al. Renal dysfunction as a predictor of stroke and systemic embolism in patients with nonvalvular atrial fibrillation: validation of the R(2)CHADS(2) index in the ROCKET AF (Rivaroxaban Once-daily, oral, direct factor Xa inhibition Compared with vitamin K antagonism for prevention of stroke and Embolism Trial in Atrial Fibrillation) and ATRIA (AnTicoagulation and Risk factors In Atrial fibrillation) study cohorts. Circulation. 2013;127:224–232.
  • Pastori D, Pignatelli P, Perticone F, et al. Aspirin and renal insufficiency progression in patients with atrial fibrillation and chronic kidney disease. Int J Cardiol. 2016;223:619–624.
  • Violi F, Pastori D, Perticone F, et al. Relationship between low Ankle-Brachial Index and rapid renal function decline in patients with atrial fibrillation: a prospective multicentre cohort study. BMJ Open. 2015;5:e008026.
  • Roldan V, Marin F, Fernandez H, et al. Renal impairment in a “real-life” cohort of anticoagulated patients with atrial fibrillation (implications for thromboembolism and bleeding). Am J Cardiol. 2013;111:1159–1164.
  • Shroff GR. NOAC dosing in atrial fibrillation and renal dysfunction: what measure are you using? J Am Coll Cardiol. 2017;70:2733–2734.
  • Shields AM, Lip GY. Choosing the right drug to fit the patient when selecting oral anticoagulation for stroke prevention in atrial fibrillation. J Intern Med. 2015;278:1–18.
  • Nishimura M, Hsu JC. Non-vitamin K antagonist oral anticoagulants in patients with atrial fibrillation and end-stage renal disease. Am J Cardiol. 2018;121:131–140.
  • Bohula EA, Giugliano RP, Ruff CT, et al. Impact of renal function on outcomes with edoxaban in the ENGAGE AF-TIMI 48 trial. Circulation. 2016;134:24–36.
  • Violi F, Soliman EZ, Pignatelli P, et al. Atrial fibrillation and myocardial infarction: a systematic review and appraisal of pathophysiologic mechanisms. J Am Heart Assoc. 2016;5:e003347.
  • Pastori D, Pignatelli P, Angelico F, et al. Incidence of myocardial infarction and vascular death in elderly patients with atrial fibrillation taking anticoagulants: relation to atherosclerotic risk factors. Chest. 2015;147:1644–1650.
  • Lamberts M, Gislason GH, Lip GY, et al. Antiplatelet therapy for stable coronary artery disease in atrial fibrillation patients taking an oral anticoagulant: a nationwide cohort study. Circulation. 2014;129:1577–1585.
  • Hohnloser SH, Oldgren J, Yang S, et al. Myocardial ischemic events in patients with atrial fibrillation treated with dabigatran or warfarin in the RE-LY (Randomized Evaluation of Long-Term Anticoagulation Therapy) trial. Circulation. 2012;125:669–676.
  • Darwiche W, Bejan-Angoulvant T, Angoulvant D, et al. Risk of myocardial infarction and death in patients with atrial fibrillation treated with dabigatran or vitamin K antagonists. Meta-analysis of observational analyses. Thromb Haemost. 2016;116:1150–1158.
  • Lip GY, Windecker S, Huber K, et al. Management of antithrombotic therapy in atrial fibrillation patients presenting with acute coronary syndrome and/or undergoing percutaneous coronary or valve interventions: a joint consensus document of the European Society of Cardiology Working Group on Thrombosis, European Heart Rhythm Association (EHRA), European Association of Percutaneous Cardiovascular Interventions (EAPCI) and European Association of Acute Cardiac Care (ACCA) endorsed by the Heart Rhythm Society (HRS) and Asia-Pacific Heart Rhythm Society (APHRS). Eur Heart J. 2014;35:3155–3179.
  • Airaksinen KE, Gronberg T, Nuotio I, et al. Thromboembolic complications after cardioversion of acute atrial fibrillation: the FinCV (Finnish CardioVersion) study. J Am Coll Cardiol. 2013;62:1187–1192.
  • Itainen S, Lehto M, Vasankari T, et al. Non-vitamin K antagonist oral anticoagulants in atrial fibrillation patients undergoing elective cardioversion. Europace. 2018;20:565–568.
  • Hansen ML, Jepsen RM, Olesen JB, et al. Thromboembolic risk in 16 274 atrial fibrillation patients undergoing direct current cardioversion with and without oral anticoagulant therapy. Europace. 2015;17:18–23.
  • Flaker G, Lopes RD, Al-Khatib SM, et al. Efficacy and safety of apixaban in patients after cardioversion for atrial fibrillation: insights from the ARISTOTLE Trial (Apixaban for Reduction in Stroke and Other Thromboembolic Events in Atrial Fibrillation). J Am Coll Cardiol. 2014;63:1082–1087.
  • Okishige K, Nakamura T, Aoyagi H, et al. Comparative study of hemorrhagic and ischemic complications among anticoagulants in patients undergoing cryoballoon ablation for atrial fibrillation. J Cardiol. 2017;69:11–15.
  • Zhao Y, Yang Y, Tang X, et al. New oral anticoagulants compared to warfarin for perioperative anticoagulation in patients undergoing atrial fibrillation catheter ablation: a meta-analysis of continuous or interrupted new oral anticoagulants during ablation compared to interrupted or continuous warfarin. J Interv Card Electrophysiol. 2017;48:267–282.
  • Yamaji H, Murakami T, Hina K, et al. Safety and efficacy of underdosing non-vitamin K antagonist oral anticoagulants in patients undergoing catheter ablation for atrial fibrillation. J Cardiovasc Pharmacol. 2017;69:118–126.
  • Cardoso R, Knijnik L, Bhonsale A, et al. An updated meta-analysis of novel oral anticoagulants versus vitamin K antagonists for uninterrupted anticoagulation in atrial fibrillation catheter ablation. Heart Rhythm. 2018;15:107–115.
  • Wu S, Yang YM, Zhu J, et al. Meta-analysis of efficacy and safety of new oral anticoagulants compared with uninterrupted vitamin K antagonists in patients undergoing catheter ablation for atrial fibrillation. Am J Cardiol. 2016;117:926–934.
  • Calkins H, Willems S, Gerstenfeld EP, et al. Uninterrupted dabigatran versus warfarin for ablation in atrial fibrillation. N Engl J Med. 2017;376:1627–1636.
  • Armbruster HL, Lindsley JP, Moranville MP, et al. Safety of novel oral anticoagulants compared with uninterrupted warfarin for catheter ablation of atrial fibrillation. Ann Pharmacother. 2015;49:278–284.
  • Cappato R, Marchlinski FE, Hohnloser SH, et al. Uninterrupted rivaroxaban vs. uninterrupted vitamin K antagonists for catheter ablation in non-valvular atrial fibrillation. Eur Heart J. 2015;36:1805–1811.
  • Ezekowitz MD, Pollack CV, Sanders P, et al. Apixaban compared with parenteral heparin and/or vitamin K antagonist in patients with nonvalvular atrial fibrillation undergoing cardioversion: Rationale and design of the EMANATE trial. Am Heart J. 2016;179:59–68.
  • ACC. 2017; Available from: http://www.acc.org/latest-in-cardiology/articles/2017/08/16/13/25/mon11am-emanate-apixaban-warfarin-afib-cardioversion-esc-2017
  • EHRA (European Heart Rhythm Association) Congress 2018, Late-breaking trials session 20.03.2018, 8:30–10:00, Abstract. Available from: https://www.escardio.org/The-ESC/Press-Office/Press-releases/Apixaban-is-a-safe-alternative-to-warfarin-during-catheter-ablation-of-atrial-fi
  • Wang KL, Lip GY, Lin SJ, et al. Non-vitamin K antagonist oral anticoagulants for stroke prevention in Asian patients with nonvalvular atrial fibrillation: meta-analysis. Stroke 2015;46:2555–2561.
  • Hori M, Connolly SJ, Ezekowitz MD, et al. Efficacy and safety of dabigatran vs. warfarin in patients with atrial fibrillation-sub-analysis in Japanese population in RE-LY trial. Circ J. 2011;75:800–805.
  • Kodani E, Atarashi H, Inoue H, et al. Beneficial effect of non-vitamin K antagonist oral anticoagulants in patients with nonvalvular atrial fibrillation – results of the J-RHYTHM registry 2. Circ J. 2016;80:843–851.
  • Chan YH, Yen KC, See LC, et al. Cardiovascular, bleeding, and mortality risks of dabigatran in Asians with nonvalvular atrial fibrillation. Stroke. 2016;47:441–449.
  • Cha MJ, Choi EK, Han KD, et al. Effectiveness and safety of non-vitamin K antagonist oral anticoagulants in Asian patients with atrial fibrillation. Stroke. 2017;48:3040–3048.
  • Li WH, Huang D, Chiang CE, et al. Efficacy and safety of dabigatran, rivaroxaban, and warfarin for stroke prevention in Chinese patients with atrial fibrillation: the Hong Kong Atrial Fibrillation Project. Clin Cardiol. 2017;40:222–229.
  • Chan YH, Kuo CT, Yeh YH, et al. Thromboembolic, bleeding, and mortality risks of rivaroxaban and dabigatran in Asians with nonvalvular atrial fibrillation. J Am Coll Cardiol. 2016;68:1389–1401.
  • Connolly SJ, Eikelboom J, Joyner C, et al. Apixaban in patients with atrial fibrillation. N Engl J Med. 2011;364:806–817.
  • Beyer-Westendorf J, Camm AJ, Coleman CI, et al. Rivaroxaban real-world evidence: validating safety and effectiveness in clinical practice. Thromb Haemost. 2016;116(Suppl. 2):S13–S23.
  • Freedman B, Lip GY. “‘Unreal world’ or ‘real world’ data in oral anticoagulant treatment of atrial fibrillation”. Thromb Haemost. 2016;116:587–589.
  • Halvorsen S, Atar D, Yang H, et al. Efficacy and safety of apixaban compared with warfarin according to age for stroke prevention in atrial fibrillation: observations from the ARISTOTLE trial. Eur Heart J. 2014;35:1864–1872.

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