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Lancet. 2013 Mar 9;381(9869):805-16.

Long-term effects of continuing adjuvant tamoxifen to 10 years versus stopping at 5 years after diagnosis of oestrogen receptor-positive breast cancer: ATLAS, a randomised trial.

Collaborators (1271)

Davies C, Sayer J, Collett V, Crowther J, Radley A, Delmestri A, Godwin J, Wang Y, Gray R, Pan H, Peto R, Beighton A, Forster M, Headon A, Hope C, Knight S, McGale P, Mozley S, Monaghan H, Muldal A, Naughten A, Turner S, Souhami R, Doll R, Altman D, Baum M, Collins R, Pritchard KI, Simpson D, Dickersin K, Arriagada R, Raina V, Williams C, Goldhirsch A, Abraham M, Chacón R, Perna F, Abud HA, Alasino CM, Algamiz CA, Alvarado Velloso JA, Alvarez AM, Alvarez Gardiol A, Alvarez Gardiol E, Arca R, Arocena H, Barbera LA, Bas C, Benitez Gil AJ, Brown Arnold M, Bustos AO, Cedaro LB, Cigno EL, Colo FA, Colombo Berra A, Coppola FS, Delia R, Dominguez ME, Fages M, Fein LE, Genovese AN, Giacomi NA, Giacomi I, Gomez I, Gonzalez Vera E, Hannois A, Hunis AP, La Palma N, Levy DE, Machiavelli MR, Marantz A, Matwiejuk MJ, Morante MS, Paleta C, Pascon GV, Pascual ME, Pejko EJ, Requejo HR, Rodriguez Md, Rodriguez Nievas O, Rossi A, Santos RL, Scalbi S, Sousa Martinez F, Staringer JC, Verdier OJ, Vigo SA, Zunino S, Forbes JF, Davis SR, Lindsay D, Bradbury J, Abdelaal AS, Abdi E, Ackland S, Ahern V, Atkinson C, Babington S, Baker C, Barker P, Baron-Hay S, Beale P, Beevors M, Begbie S, Beith J, Bell D, Bell R, Benjamin C, Birks D, Blum R, Bonaventura A, Bond R, Boyce A, Boyer M, Boyle F, Bradbury J, Brigham B, Bright N, Burcombe R, Byard I, Byram D, Castles L, Childs J, Chipman M, Chirgwin J, Coates A, Cox S, Craft P, de Boer R, Delaney G, Della-Fiorentin S, Dewar J, Donnelly P, Eastman M, Evans B, Falkov A, Fitzharris B, Francis M, Freund J, Friedlander M, Gas H, Gauden S, Gebski V, Gillette D, Goldrick A, Goldstein D, Gourlay R, Green A, Gregory P, Grygiel J, Gunn I, Haines I, Harnett P, Harris M, Harrup R, Hart S, Harvey V, Hastrich D, Hayden A, Hemanth T, Hickey B, Holocek M, Hughes M, Humeniuk V, Ingram D, Iseli A, Jackson D, Jacob G, Jamieson A, Jeffery M, Jose C, Kannourakis G, Kay RG, Kiffer J, Krawitz H, Leong D, Levy R, Lewis C, Linacre R, Lipton L, Logan D, Lowenthal R, Lynch R, Macnab L, Maguire E, Marx G, Masters R, McCrystal M, McKendrick J, McLeay B, McLennan R, Mercer P, Mitchell G, Mitchell P, Moylan E, Pavlakis N, Porges S, Porter D, Porter I, Porter T, Pyke C, Robinson B, Rutovitz J, Sardelic F, Schwarz M, Scott B, Segelov E, Sillar R, Simes JR, Smee B, Smith T, Spry N, Stanley R, Stewart JF, Stewart J, Stoney D, Sullivan A, Sunderland K, Thompson P, Thornton D, Tin M, Townend D, Turner S, Underhill C, van Hazel G, Walsh DC, Wheeler H, White K, White S, Wynne C, Young A, Young R, Kostetskaya T, Piccart M, Bartholemus S, Awada A, Cardoso F, Closon M, Cocquyt DV, Coucke P, DeFoort P, Deleu I, Depypere DH, Everaert E, Geurs F, Kains J, Neven P, Serreyn DR, van den Broecke R, Alencar VH, Silva HM, Vieira Ed, Almeida W Jr, Alves Barbosa O, Araujo SS, Archangelo I Jr, Arruda I, Nogueira Barreira C, Batista Lucena J, Bezerra Pinheiro G, Caleffi M, Campos Avelar JT, Coutinho Maia Silva Vd, Cronemberger EE, Diogenes AB, Emiliano VR, d Freitas R, d Freitas Torres A, Farias R, Freitas MD, Funke MA, Fuschino C, d Gama Dantes D, Gaspar C, Hoffman E, Juacaba SF, Lopes Marques SH, Lorenzato F, Maroja A, Maroja R, Marques E, Matias Md, Medeiros GP, Melo PH, Miranda Henriques FA, Monteiro M, Mourao de Farias JW, Moura J, Mousinho AP, Murad AM, Murillo Britto L, Nonata d Andrade AA, Pascoto P, Peixoto J, Peixoto Lima G, Pereira MA, Pinheiro Gd, Prado Wanderley T, Reis JH, Ribeiro RA, Ritter V, Sales RM, Alencar MS, Santiago Almeida R, Stenger N, Studart Leal C, Tosello de Oliveira C, Vianna LL, Zerbini S, Coelho d Sá D, guiar Porto IA, d Moraes GA, Peralta O, Müller B, Arriagada R, Acevedo EA, Acevedo JC, Arevalo RO, Baeza R, Belmar A, Bravo ME, Bronfman L, Camacho J, Campos M, Cardemil B, Carvajal P, Cerda B, Cisternas F, Contreras E, Cornejo JF, Cubillos AJ, del Castillo C, Escobar P, Fernández M, Fica A, Fritis M, Gambi G, Giannini O, Gomez LS, Gutiérrez J, Hales C, Hasbún R, Huidobro P, Iglesis R, Jury OS, Krause H, Lagos JM, León A, León M, Madrid J, Mariani C, Martínez Lepe R, Martínez Rogers R, Matamala LA, Moreno D, Núñez P, Olcesse A, Olfos P, Orlandi L, Ortúzar W, Pabst Y, Paredes H, Pérez E, Pierart J, Pineda V, Pinto A, Pizarro Z, Rey G, Rivas O, Rodríguez M, Rojas H, Rosas J, Ruíz de Viñaspre P, Russo JM, San Martín S, Sepúlveda L, Solé J, Steinberg J, Toledo M, Torres C, Torres JM, Torres R, Torres S, Uribe A, Valenzuela M, Vásquez C, Vigneaux IM, Vigueras G, Vila A, Villagrán H, Villalón M, Zambrano V, Zlatar Z, Zúñiga M, Shao Y, Wang X, Wang Y, Fan F, Gong YP, Huang JL, Jin ZH, Li WL, Lin ZW, Liu HJ, Liu P, Liu QL, Ma XT, Pang D, Qiao XM, Shi KD, Sun YQ, Wang L, Wang YZ, Wu T, Xie ZB, Zhang B, Zhang WQ, Zhao HP, Zhou WP, Zhu JB, Ramirez C, Castro C, Vrbanec D, Herceg D, Juretic A, Martinovic I, Paulinic-Diminic V, Pezerovic DE, Plestina S, Alvarez RI, Amador RM, Arbesu MA, Ballesta L, Catala M, de la Torre A, Domecq M, Escobar X, Franco S, O'Farril M, Perez I, Reyes de la Paz A, Rodriguez I, Rodriguez R, Sanchez I, Soriano JL, Valdes Z, Petruzelka L, Pribylova O, Adamkova-Krakorova D, Ambrus M, Barkmanova J, Barsova L, Bartos J, Bednarik O, Benesova V, Brychta M, Brychtova M, Cahova S, Chodacka M, Chovanec J, Cmejlova V, Coupek P, Cwiertka K, Finek J, Hacklova M, Hanus L, Helmichova E, Holikova M, Holub J, Honova H, Hovorkova K, Hrabetova P, Hubnerova P, Hudinkova L, Justrova D, Kankova H, Karasek P, Kaspar M, Kindlova E, Kiss I, Kocak I, Kohoutek M, Kolarova I, Konopaisek B, Kozak JT, Kozevnikovova R, Kozisek L, Krasna L, Krizan K, Kubackova K, Kubecova M, Kuta M, Lemez P, Lorenz I, Loukotkova L, Lukesova S, Lysy M, Macharova H, Mackova D, Mares P, Martin S, Muller V, Neumanova R, Novy F, Ostrizkova L, Pavel Pavlov L, Pluhacek S, Prausova J, Pribylova J, Ruzickova J, Safanda M, Salvet J, Sedlackova E, Semonska S, Seneklova Z, Smakal M, Soumarova M, Spelda S, Spurny V, Strzondala W, Tesarova P, Tomancova V, Tomanova M, Trskova K, Vesela H, Vondrackova K, Vydra J, Vyzula R, Zemanova M, Zimovjanova M, Zvolsky M, Khaled H, Badran A, Abd-Elmoneim Khalil SE, Abu Taleb F, Badran A, El Akkad H, El-Khodary A, Gaafar RM, Gad El Mawla N, Hablas A, Ismail K, Moneer M, Zaghloul MS, Ratsep V, Valvere V, Kurvet A, Kutner R, Vahter L, Bernard P, Hill C, Alexopoulos C, Razis E, Kwan WH, Au GK, Chan P, Chan RT, Cheng A, Chi Kin C, Foo W, Cheng HC, Kwok C, Kwong D, Leung C, Leung WL, Liu King Yin R, Luk MY, Ngan RK, Siu SW, Suen J, Tong CC, Tong M, Tung SY, Yau TK, Yiu H, Raina V, Mittra I, Advani SH, Badwe RA, Bakane BC, Bandyopadhyay MN, Chandrasekharan A, Chaturvedi A, D'Cruz AK, Deka AC, Digumarti R, Dinesh M, Dinshaw KA, Doshi JP, Durgaprasad G, Gopal R, Gupta VK, Hawaldar R, Jain S, Jayakumar K, Joharapurkar SR, John S, Julka PK, Khanna R, Kothari KC, Kumar MV, Kumar S, Madhu C, Mathew A, Mathew BS, Mathor B, Mehta A, Mehta F, Mehta G, Misra NC, Misra S, Nalini Y, Panchal HP, Parekh B, Parmar V, Parshad R, Patel DD, Patel V, Premkumar S, Radhika R, Rajan B, Sarkar SK, Seenu V, Sengupta A, Shah P, Sharma A, Sharma SC, Shenoy KK, Shukla HS, Shukla NK, Shukla SN, Singh A, Singh KK, Srivastava A, Subrahmaniyam K, Sur PK, Tongaonkar HB, Vashisht R, Veerendra Kumar KV, Vijaya S, Haddad P, Dehshiri K, Amouzgar-Hashemi F, Madani H, Mortazavi SH, Mousavizadeh MA, Raafat J, Sadrolhefazi B, Tabatabaeefar M, Finnegan T, Inbar M, Ben-Baruch N, Shani A, Barak F, Ben-Zui N, Catane R, Dinerman M, Evron E, Figer A, Gips M, Hayat H, Idelevich E, Isacson R, Kopp V, Kovner F, Marchasin L, Matcejevsky D, Olga L, Perepechi E, Ron IG, Safra T, Sarid D, Shlanger S, Shumeli E, Tepper E, Yaal-Hahoshen N, Nicolucci A, Valentini M, Amiconi G, Ascione F, Banducci S, Baratelli G, Battistelli F, Bianchi R, Bravi S, Chiara A, Dall'Omo B, De Matteis A, Di Costanzo F, Di Lullo L, di Nardo B, Ferrari S, Fiore R, Fornari G, Gini G, Giordano M, Giovannini M, Gravina A, Isa L, Laudadio L, Luchena G, Mantovani G, Marcellini M, Mari E, Marpicati P, Martoni A, Massa E, Molino AM, Nuzzo A, Pedersini R, Piana E, Pinna NL, Pirozzoli MC, Recchia F, Riccardi A, Robbiati FS, Rossi E, Sannicoló M, Ucci G, Valli MC, Zamagni C, Ohashi Y, Ikeda T, Nomura Y, Yoshida E, Akashi S, Aogi K, Arita E, Aoyama H, Emi A, Fujisawa J, Fujiwara K, Fukutomi T, Haruta R, Hata Y, Hayashida T, Hojo T, Hozumi Y, Inoue H, Ishida K, Ishida M, Kanbayashi C, Kanke D, Kataoka A, Kato A, Kato N, Katsumata N, Kawabuchi Y, Kawaguchi H, Kitajima M, Kobayashi S, Kodaira M, Koga C, Mitsuyama S, Miyauchi M, Mori E, Murakami S, Nagao K, Nakamura Y, Nishimura S, Nishimura R, Ohba M, Onishi T, Ohno S, Osako T, Osumi S, Sakata M, Sano M, Sato T, Sato Y, Shigematsu H, Takahashi H, Takahashi Y, Takashima S, Takenaka H, Tamae K, Tanaka K, Toge T, Toi M, Uchida Y, Uchiyama N, Yamaguchi H, Yamamoto N, Yamashita H, Yoshiyama T, Berzins J, Bitina M, Gailite I, Keire G, Purkalne T, Ratiani M, Zvirbule Z, Valuckas K, Aizenas M, Andzeviciene D, Caropaite V, Cesas A, Ciceniene A, Juodzbaliene E, Kurtinaitis J, Luksyte A, Satkauskiene N, Smailyte G, Tamoshaitite L, Zlabiene A, Zinser J, Erazo Valle A, Maafs E, Ramirez MT, Rutgers E, Dalesio O, Wever L, Algie G, Baars JW, Belderbos J, Boom R, Brakenhoff JA, Dalesio O, de Swart CA, de Valk B, Harskamp V, Leeksma OC, Roozendaal KJ, Schrama J, Tanka AK, Terpstra WE, Van Coevorden F, van Geldere D, Veen H, Veltkamp SC, Voogt P, Raina V, Bahrani BA, Abed R, Pienkowski T, Rubach MT, Kielanowska J, Bassara H, Boguszewska D, Brandys A, Brewczynska E, Chudzik M, Czyzewska K, Debicka I, Dobielinska-Eliszews T, Filipczyk-Cisarz E, Foszczynska-Kloda M, Frackowiak L, Garncarek A, Giermek J, Glinka-Malasnicka E, Gornas M, Hajdukiewicz W, Hudziec P, Jagiello-Gruszfeld A, Jonca M, Karczmarek-Borowska B, Kielanowska J, Koralewski P, Koscianska B, Kucharska A, Kukawski P, Kurianowicz MM, Litwiniuk M, Marczak-Zietkiewicz M, Muchacki R, Oberc J, Pajak K, Pawlaczyk A, Perual J, Pienkowski A, Piskorski W, Pysz M, Rubach M, Rutkowski R, Sikorska M, Smietana A, Songin A, Stolarek M, Stopyra G, Suszko-Kazarnowicz M, Szybicka-Fliskowska E, Talerczyk M, Walaszkowska A, Warzocha K, Wawrzynczak B, Wegrzyn J, Wlonska-Kusy B, Wojtacki J, Zabkowska K, Zielezinska A, Ziemba BA, Zuziak D, Zygulski I, Gervasio H, Albano JE, Carvalho T, Madeira P, Pazos I, Semiglazov V, Barash N, Beljakov S, Bozhok A, Bulavina I, Burdaeva O, Cheporev SV, Cherenkova M, Chissov V, Churilova LA, Dmitrina H, Feodorov K, Fisanovich T, Gorbounova vA, Ivanova O, Koroleva LA, Kozhevnikov S, Lazarev A, Luppov V, Magcoeva L, Manikhas G, Melnikov D, Orlova R, Petrova V, Pogodina E, Predit V, Raevskaya N, Ricova T, Roman L, Seleznjeva I, Shomova MV, Sidorov SV, Spheglov J, Svetlouno P, Talovskiy J, Vtoraya OM, Murray E, Dent D, Bental N, Claus R, Cox C, Giles S, Gudgeon A, Hemus A, McEvoy E, Mokone DH, Moodley D, Mundawarara S, Paris G, Pokharel B, Rapoport BL, Ruff P, Salton D, Sebastian E, Shelley A, Simonds H, Sitas F, Tarr A, Tarukandirwa C, van Wijk AL, Werner ID, Bonfill X, Urrútia G, Martinez EC, Tort S, Abrio MV, Adansa C, Aguiar Morales J, Albero A, Alfaro J, Alija V, Almenar Cubells D, Alonso C, Alonso Amigo A, Alonso Curbera G, Alonso Redondo E, Alvarez I, Andrade Santiago J, Andrés R, Antolín Novoa S, Antón MI, Arcusa Lanza MA, Arrivi A, Avellà A, Avellanal Barral JP, Badia i Canto MA, Ballesteros Garcia P, Barros Md, Bastús-Piulats R, Batista López JN, Batiste-Alentorn E, Belón Carrión J, Benavides M, Bernabé Caro R, Blanco Guerrero R, Bohn Sarmiento U, Boleda M, Bosch C, Bretón Garcia JJ, Burillo Cordero MA, Buxó i Costa J, Calvo E, Calvo L, Capdevila F, Carabantes FJ, Cardona Hernández T, Carrasco E, Casado J, Casas A, Catot Tort S, Chacón López-Muñiz JI, Chaves Conde M, Cirera i Noguera L, Ciruelos E, Colomer R, Cruz J, De la Cruz MA, De La Cruz L, De La Cueva H, Del Moral R, Domènech M, Dominguez Cunchillos F, Donay O, Dorta Delgado J, Duque Amusco A, Escobedo A, España Saz P, Espinosa Arranz E, Esteban Esteban C, Etxeberria A, Fabregat Mayol X, Falo C, Fernández Bautista E, Fernández Ortega A, Fonseca Sánchez E, Franquesa Granell RM, Gallardo E, Gallego O, Gallurt Moreira P, García M, García Carbonero I, García López MJ, García Pérez M, Garrido Saldana A, Garrigós L, Gay M, Germà Lluch JR, Gil M, Giménez U, Gómez Bernal A, González B, González Del Alba A, González Del Val R, González de Sande LM, González Mancha R, Gordon M, Gravalos Castro C, Guasch i Jordan I, Guillot M, Hornedo J, Iglesias Pérez L, Isla MD, Izquierdo MA, Jiménez Orozco E, Jolis López L, Juez I, Laín JM, Lasso de la Vega R, Limón ML, Llanos M, López P, López Gómez LJ, López López JJ, Lorenzo Penuel A, Lozano Barriuso AM, Llorente R, Manzano H, Martín Broto J, Martínez B, Martínez del Prado P, Martín García G, Mendiola C, Molina F, Molins C, Montano A, Montesinos J, Moreno Nogueira JA, Múñoz J, Múñoz M, Muñoz Madero V, Murillo MT, Nogué M, Noguer M, Ojeda B, Olmos S, Oramas J, Palomar L, Pastor P, Pérez Carrión R, Pérez Escutia MA, Pérez Olaguer J, Pérez Pérez Md, Pérez-Regadera Gómez J, Pericay C, Petrement Briones J, Piera Pibernat JM, Plazaola A, Rifà J, Rivero JA, Rodríguez A, Rodríguez JM, Rodríguez López R, Rodríguez Navarro P, Roget M, Ruiz Borrego M, Saenz A, Safiz J, Saigí E, Sala González MA, Salas Buzón C, Saldana J, Salgado M, Sanahuja V, Sánchez Ruiz A, Sanz Lacalle J, Sanz Martín M, Satrústegi JJ, Schneider J, Seguí MA, Servitja S, Sureda González M, Terrasa J, Tres Sánchez A, Tusquets I, Urrútia G, Valentín V, Valladares Ayerbes M, Vázquez S, Velasco A, Vicente P, Villanueva MJ, Virizuela Echaburu J, Zamora Aunon P, Hou MF, Chen KM, Chung CY, Du SS, Huang CS, Kok VC, Kuo SJ, Lin C, Tu SH, Soong YG, Zhang JY, Rahal K, Topuzlu C, Aslay I, Baltali DE, Berberoglu U, Bolukbusi H, Buyukunal E, Camlibel S, Dincer M, Erkocak EU, Ozdedeli DE, Ozturk N, De Souza C, Harris LD, Afrookteh AJ, Allgaier W, Andrade R, Arevalos A, Armstrong K, Barnes A, Barnes H, Barnes SG, Bazeley SP, Blum R, Bowles R, Branton S, Breslin ML, Bryant DS, Bryant DW, Bullock R, Campana T, 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Author information

  • 1Clinical Trial Service Unit and Epidemiological Studies Unit, University of Oxford, UK.

Erratum in

  • Lancet. 2013 Mar 9;381(9869):804.

Abstract

BACKGROUND:

For women with oestrogen receptor (ER)-positive early breast cancer, treatment with tamoxifen for 5 years substantially reduces the breast cancer mortality rate throughout the first 15 years after diagnosis. We aimed to assess the further effects of continuing tamoxifen to 10 years instead of stopping at 5 years.

METHODS:

In the worldwide Adjuvant Tamoxifen: Longer Against Shorter (ATLAS) trial, 12,894 women with early breast cancer who had completed 5 years of treatment with tamoxifen were randomly allocated to continue tamoxifen to 10 years or stop at 5 years (open control). Allocation (1:1) was by central computer, using minimisation. After entry (between 1996 and 2005), yearly follow-up forms recorded any recurrence, second cancer, hospital admission, or death. We report effects on breast cancer outcomes among the 6846 women with ER-positive disease, and side-effects among all women (with positive, negative, or unknown ER status). Long-term follow-up still continues. This study is registered, number ISRCTN19652633.

FINDINGS:

Among women with ER-positive disease, allocation to continue tamoxifen reduced the risk of breast cancer recurrence (617 recurrences in 3428 women allocated to continue vs 711 in 3418 controls, p=0·002), reduced breast cancer mortality (331 deaths vs 397 deaths, p=0·01), and reduced overall mortality (639 deaths vs 722 deaths, p=0·01). The reductions in adverse breast cancer outcomes appeared to be less extreme before than after year 10 (recurrence rate ratio [RR] 0·90 [95% CI 0·79–1·02] during years 5–9 and 0·75 [0·62–0·90] in later years; breast cancer mortality RR 0·97 [0·79–1·18] during years 5–9 and 0·71 [0·58–0·88] in later years). The cumulative risk of recurrence during years 5–14 was 21·4% for women allocated to continue versus 25·1% for controls; breast cancer mortality during years 5–14 was 12·2% for women allocated to continue versus 15·0% for controls (absolute mortality reduction 2·8%). Treatment allocation seemed to have no effect on breast cancer outcome among 1248 women with ER-negative disease, and an intermediate effect among 4800 women with unknown ER status. Among all 12,894 women, mortality without recurrence from causes other than breast cancer was little affected (691 deaths without recurrence in 6454 women allocated to continue versus 679 deaths in 6440 controls; RR 0·99 [0·89–1·10]; p=0·84). For the incidence (hospitalisation or death) rates of specific diseases, RRs were as follows: pulmonary embolus 1·87 (95% CI 1·13–3·07, p=0·01 [including 0·2% mortality in both treatment groups]), stroke 1·06 (0·83–1·36), ischaemic heart disease 0·76 (0·60–0·95, p=0·02), and endometrial cancer 1·74 (1·30–2·34, p=0·0002). The cumulative risk of endometrial cancer during years 5–14 was 3·1% (mortality 0·4%) for women allocated to continue versus 1·6% (mortality 0·2%) for controls (absolute mortality increase 0·2%).

INTERPRETATION:

For women with ER-positive disease, continuing tamoxifen to 10 years rather than stopping at 5 years produces a further reduction in recurrence and mortality, particularly after year 10. These results, taken together with results from previous trials of 5 years of tamoxifen treatment versus none, suggest that 10 years of tamoxifen treatment can approximately halve breast cancer mortality during the second decade after diagnosis.

FUNDING:

Cancer Research UK, UK Medical Research Council, AstraZeneca UK, US Army, EU-Biomed.

Comment in

PMID:
23219286
[PubMed - indexed for MEDLINE]
PMCID:
PMC3596060
Free PMC Article

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