Supportive Care in Cancer

, Volume 26, Issue 4, pp 1253–1264 | Cite as

Fatigue- and health-related quality-of-life in anemic patients with lymphoma or multiple myeloma

  • Pere Gascón
  • Reyes Arranz
  • Joan Bargay
  • Fernando Ramos
Original Article



The purpose of this study was to describe perceptions of fatigue in anemic patients with lymphoma or multiple myeloma (MM).


This is an observational multicenter study in a prospective cohort of lymphoma and MM patients with hemoglobin ≤ 11 g/dl managed under clinical practice. Fatigue was assessed at baseline and after 3 months using the PERFORM questionnaire, the Functional Assessment of Cancer Therapy-Fatigue, the linear analogue self-assessment, and visual analogue scale (VAS) scales.


Two hundred and fifty patients (125 with lymphoma, 125 with MM) were included. Only 59.2 and 56.0% of patients received treatment for anemia, respectively. After 3 months, the hemoglobin levels increased significantly compared to baseline from 10.0 ± 1.2 to 11.5 ± 1.8 in the lymphoma group and from 9.9 ± 0.9 to 10.9 ± 1.5 g/dl, in the MM group (P < 0.001, both comparisons). At baseline, 87.2 and 84.8% of patients had fatigue (median intensity (VAS) 60 and 50). The overall PERFORM score decreased from 35.2 ± 15.2 to 32.0 ± 14.6 (P = 0.048), without differences between groups. No statistically significant changes were observed in the other scales. After multivariable adjustment, the only common independent factor associated to improvements in fatigue and health-related quality-of-life (HRQoL) was an increase in hemoglobin levels. The administration of curative intention treatment was also associated with HRQoL improvements. The psychometric properties of the PERFORM questionnaire in MM patients were good (Cronbach’s alpha 0.87–0.98; intraclass correlation coefficients 0.84–0.89; effect sizes 0.59–0.96).


Almost all patients with lymphoma or MM diagnosed with anemia suffered from fatigue of moderate to severe intensity. Despite similar anemia supportive treatment, better correction of fatigue scores was observed in lymphoma patients after 3 months. Increases in hemoglobin were significantly associated to improvements in fatigue and HRQoL.


Fatigue Anemia Lymphoma Multiple myeloma Quality-of-life Questionnaire 



Writing assistance was supported by Amgen S.A. and provided by Dr. Neus Valveny from Trial Form Support, who wrote the first draft. The authors wish to acknowledge Ariadna Lloansí (Amgen S.A.) for the critical review of the manuscript and Amgen S.A. for financial support of this study. The conclusions, interpretations, and opinions expressed herein are those of the authors.

PERFORM V Study Group: Dr. Abelardo Bárez Garcia, Hospital Nuestra Señora de Sonsoles, Ávila, Spain; Dr. Antonio Salar, Hospital del Mar, Barcelona, Spain; Dra. Asunción Mora Casado, Hospital Universitario Infanta Sofía, San Sebastián de los Reyes, Spain; Dra. Carme Talarn Forcadell, Hospital Universitari Joan XXIII, Tarragona, Spain; Dra. Cristina Encinas Rodriguez, Hospital General Universitario Gregorio Marañón, Madrid, Spain; Dra. Emma Lopez Abadia, Hospital General Universitario de Elche, Elche, Spain; Dr. Fernando Escalante Barrigon, Hospital Universitario de León, León, Spain; Dra. Francisca Hernández, Hospital Universitario San Cecilio, Granada, Spain; Dra. Francisca Marín Jimenez, Hospital General Universitario de Elche, Elche, Spain; Dr. Javier De La Rubia, Hospital Universitari i Politècnic La Fe, Valencia, Spain; Dr. Joan Bargay, Hospital Son Llàtzer, Palma de Mallorca, Spain; Dr. Juan José Lahuerta, Hospital Universitario Doce de Octubre, Madrid, Spain; Dr. Juan-Nicolas Rodriguez Rodriguez, Hospital Juan Ramón Jimenez, Huelva, Spain; Dra. Asunción Echeveste Gutierrez, Hospital Universitario Donostia, San Sebastián, Spain; Dra. María Victoria Moreno Romero, Hospital Juan Ramón Jimenez, Huelva, Spain; Dra. Mercedes Gironella, Hospital Universitari Vall D’Hebron, Barcelona, Spain; Dr. Miguel Hernández, Hospital Clínico Universitario de Canarias, San Cristóbal de La Laguna, Spain; Dra. Pilar Lopez Garrido, Hospital Universitario Virgen de Las Nieves, Granada, Spain; Dra. Pilar Rabasa, Hospital San Pedro y San Millán, Logroño, Spain; Dra. Reyes Arranz Sáez, Hospital Universitario La Princesa, Madrid, Spain; Dr. Secundino Ferrer, Hospital Universitario Doctor Peset, Valencia, Spain; Dra. Sonia Piernas, Corporació Sanitària Parc Taulí, Sabadell, Spain; Dr. Valentín Garcia, Hospital Universitario Ramón y Cajal, Madrid, Spain; Dra. Verónica Roldan, Hospital San Pedro y San Millan, Logroño, Spain.

Author contributions

All authors designed the study, coordinated the group, supervised clinical data collection, and reviewed the analysis and the manuscript. All the authors approved the final version of the manuscript.

Funding information

This study was financially supported by Amgen S.A.

Compliance with ethical standards

The study was approved by the Ethics Committee of the Hospital Clínic de Barcelona and has been performed in accordance with the Declaration of Helsinki. Informed consent was obtained from all study participants.

Conflict of interest

Dr. Ramos reports personal fees from AMGEN during the conduct of the study and grants, personal fees, and others from CELGENE; personal fees and other from NOVARTIS; personal fees from AMGEN; personal fees from GLAXO SMITH KLINE; personal fees from PFIZER; and personal fees and other from JANSSEN, outside the submitted work. The other authors have stated that they have no conflicts of interest.

Supplementary material

520_2017_3948_MOESM1_ESM.pdf (88 kb)
ESM 1 (PDF 88 kb)


  1. 1.
    Ludwig H, Van Belle S, Barrett-Lee P, Birgegård G, Bokemeyer C, Gascón P, Kosmidis P, Krzakowski M, Nortier J, Olmi P, Schneider M, Schrijvers D (2004) The European Cancer Anaemia Survey (ECAS): a large, multinational, prospective survey defining the prevalence, incidence, and treatment of anaemia in cancer patients. Eur J Cancer 40:2293–2306. CrossRefPubMedGoogle Scholar
  2. 2.
    Canaparo R, Casale F, Muntoni E, Zara GP, Della Pepa C, Berno E, Pons N, Fornari G, Eandi M (2000) Plasma erythropoietin concentrations in patients receiving intensive platinum or nonplatinum chemotherapy. Br J Clin Pharmacol 50:146–153CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    National Comprehensive Cancer Network (2003) Cancer-related fatigue. Clinical practice guidelines in oncology. J Natl Compr Cancer Netw 1:308–331CrossRefGoogle Scholar
  4. 4.
    Gerber LH, Stout N, McGarvey C, Soballe P, Shieh C, Diao G, Springer BA, Pfalzer LA (2011) Factors predicting clinically significant fatigue in women following treatment for primary breast cancer. Support Care Cancer 19:1581–1591. CrossRefPubMedGoogle Scholar
  5. 5.
    Díaz N, Menjón S, Rolfo C, García-Alonso P, Carulla J, Magro A, Miramón J, Rodríguez CA, de Castellar R, Gasquet JA (2008) Patients’ perception of cancer-related fatigue: results of a survey to assess the impact on their everyday life. Clin Transl Oncol 10:753–757CrossRefPubMedGoogle Scholar
  6. 6.
    Barsevick A, Frost M, Zwinderman A, Hall P, Halyard M, Consortium GENEQOL (2010) I’m so tired: biological and genetic mechanisms of cancer-related fatigue. Qual Life Res 19:1419–1427. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Sprangers MA, Van Dam FS, Broersen J, Lodder L, Wever L, Visser MR, Oosterveld P, Smets EM (1999) Revealing response shift in longitudinal research on fatigue—the use of the thentest approach. Acta Oncol 38:709–718CrossRefPubMedGoogle Scholar
  8. 8.
    Jacobsen PB, Hann DM, Azzarello LM, Horton J, Balducci L, Lyman GH (1999) Fatigue in women receiving adjuvant chemotherapy for breast cancer: characteristics, course, and correlates. J Pain Symptom Manag 18:233–242CrossRefGoogle Scholar
  9. 9.
    Molassiotis A, Morris PJ (1999) Quality of life in patients with chronic myeloid leukemia after unrelated donor bone marrow transplantation. Cancer Nurs 22:340–349CrossRefPubMedGoogle Scholar
  10. 10.
    Berger AM, Farr L (1999) The influence of daytime inactivity and nighttime restlessness on cancer-related fatigue. Oncol Nurs Forum 26:1663–1671PubMedGoogle Scholar
  11. 11.
    Romito F, Montanaro R, Corvasce C, Di Bisceglie M, Mattioli V (2008) Is cancer-related fatigue more strongly correlated to haematological or to psychological factors in cancer patients? Support Care Cancer 16:943–946. CrossRefPubMedGoogle Scholar
  12. 12.
    Yennurajalingam S, Palmer JL, Zhang T, Poulter V, Bruera E (2008) Association between fatigue and other cancer-related symptoms in patients with advanced cancer. Support Care Cancer 16:1125–1130. CrossRefPubMedGoogle Scholar
  13. 13.
    Baró E, Carulla J, Cassinello J, Colomer R, Mata JG, Gascón P, Gasquet JA, Rodríguez CA, Valentín V (2011) Psychometric properties of the Perform Questionnaire: a brief scale for assessing patient perceptions of fatigue in cancer. Support Care Cancer 19:657–666. CrossRefPubMedGoogle Scholar
  14. 14.
    Gascón P, Rodríguez CA, Valentín V, Mata JG, Carulla J, Cassinello J, Colomer R, Baró E (2013) Usefulness of the PERFORM questionnaire to measure fatigue in cancer patients with anemia: a prospective, observational study. Support Care Cancer 21:3039–3049. CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Gabrilove JL, Cleeland CS, Livingston RB, Sarokhan B, Winer E, Einhorn LH (2011) Clinical evaluation of once-weekly dosing of epoetin alfa in chemotherapy patients: improvements in hemoglobin and quality of life are similar to three-times-weekly dosing. J Clin Oncol 19:2875–2882CrossRefGoogle Scholar
  16. 16.
    Patrick DL, Gagnon DD, Zagari MJ, Mathijs R, Sweetenham J (2003) Assessing the clinical significance of health-related quality of life (HrQOL) improvements in anaemic cancer patients receiving epoetin alfa. Eur J Cancer 39:335–345. CrossRefPubMedGoogle Scholar
  17. 17.
    Cartenì G, Giannetta L, Ucci G, De Signoribus G, Vecchione A, Pinotti G, Puglisi F, Contillo A, Pezzella G, Orecchia S, Beccaglia P, OBI/EPO-ITA-01/1 study group (2007) Correlation between variation in quality of life and change in hemoglobin level after treatment with epoetin alfa 40,000 IU administered once-weekly. Support Care Cancer 15:1057–1066. CrossRefPubMedGoogle Scholar
  18. 18.
    Johnsen AT, Tholstrup D, Petersen MA, Pedersen L, Groenvold M (2009) Health related quality of life in a nationally representative sample of haematological patients. Eur J Haematol 83:139–148. CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Birgegård G, Gascón P, Ludwig H (2006) Evaluation of anaemia in patients with multiple myeloma and lymphoma: findings of the European Cancer Anaemia Survey. Eur J Haematol 77:378–386. CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Prieto JM, Blanch J, Atala J, Carreras E, Rovira M, Cirera E, Gastó C (2006) Clinical factors associated with fatigue in haematologic cancer patients receiving stem-cell transplantation. Eur J Cancer 42:1749–1755. CrossRefPubMedGoogle Scholar
  21. 21.
    Gil-Fernández J, Ramos C, Tamayo T, Tomás F, Figuera A, Arranz R, Martínez-Chamorro C, Fernández-Rañada M (2003) Quality of life and psychological well-being in Spanish long-term survivors of Hodgkin’s disease: results of a controlled pilot study. Ann Hematol 82:14–18. PubMedGoogle Scholar
  22. 22.
    Straus DJ, Testa MA, Sarokhan BJ, Czuczman MS, Tulpule A, Turner RR, Riggs SA (2006) Quality-of-life and health benefits of early treatment of mild anemia: a randomized trial of epoetin alfa in patients receiving chemotherapy for hematologic malignancies. Cancer 107:1909–1917. CrossRefPubMedGoogle Scholar
  23. 23.
    Hedenus M, Adriansson M, San Miguel J, MHH K, Schipperus MR, Juvonen E, Taylor K, Belch A, Altés A, Martinelli G, Watson D, Matcham J, Rossi G, Littlewood TJ, Darbepoetin Alfa 20000161 Study Group (2003) Efficacy and safety of darbepoetin alfa in anaemic patients with lymphoproliferative malignancies: a randomized, double-blind, placebo-controlled study. Br J Haematol 122:394–403CrossRefPubMedGoogle Scholar
  24. 24.
    Baró E, Carulla J, Cassinello J, Colomer R, Mata JG, Gascón P, Gasquet JA, Herdman M, Rodríguez CA, Sánchez J, Valentín V (2009) Development of a new questionnaire to assess patient perceptions of cancer-related fatigue: item generation and item reduction. Value Health 12:130–138. CrossRefPubMedGoogle Scholar
  25. 25.
    Cella D (1997) The Functional Assessment of Cancer Therapy-Anemia (FACT-An) Scale: a new tool for the assessment of outcomes in cancer anemia and fatigue. Semin Hematol 34:13–19PubMedGoogle Scholar
  26. 26.
    Demetri GD, Kris M, Wade J, Degos L, Cella D (1998) Quality-of-life benefit in chemotherapy patients treated with epoetin alfa is independent of disease response or tumor type: results from a prospective community oncology study. Procrit Study Group. J Clin Oncol 16:3412–3425CrossRefPubMedGoogle Scholar
  27. 27.
    Mitchell SA (2010) Cancer-related fatigue: state of the science. PM R 2:364–383. CrossRefPubMedGoogle Scholar
  28. 28.
    Jacobsen PB, Donovan KA, Vadaparampil ST, Small BJ (2007) Systematic review and meta-analysis of psychological and activity-based interventions for cancer-related fatigue. Health Psychol 26:660–667. CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Luctkar-Flude MF, Groll DL, Tranmer JE, Woodend K (2007) Fatigue and physical activity in older adults with cancer: a systematic review of the literature. Cancer Nurs 30:E35–E45. CrossRefPubMedGoogle Scholar
  30. 30.
    Revicki DA, Stull D, Vernon M, Rader M, Tomita D, Viswanathan HN (2012) Assessing the effect of darbepoetin alfa on patient-reported fatigue in chemotherapy-induced anemia in four randomized, placebo-controlled clinical trials. Qual Life Res 21:311–321. CrossRefPubMedGoogle Scholar
  31. 31.
    Glaspy J (2001) Anemia and fatigue in cancer patients. Cancer 92:1719–1724CrossRefPubMedGoogle Scholar
  32. 32.
    Esquerdo G, Llorca C, Cervera JM, Orts D, Juárez A, Carrato A (2011) Effectiveness of darbepoetin alfa in a cohort of oncology patients with chemotherapy-induced anaemia. Relationship between variation in three fatigue-specific quality of life questionnaire scores and change in haemoglobin level. Clin Transl Oncol 13:341–347. CrossRefPubMedGoogle Scholar
  33. 33.
    Calabrich A, Katz A (2011) Management of anemia in cancer patients. Future Oncol 7:507–517. CrossRefPubMedGoogle Scholar
  34. 34.
    De Waele S, Van Belle S (2010) Cancer-related fatigue. Acta Clin Belg 65:378–385. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Pere Gascón
    • 1
  • Reyes Arranz
    • 2
  • Joan Bargay
    • 3
  • Fernando Ramos
    • 4
  1. 1.Hospital ClínicBarcelonaSpain
  2. 2.Hospital Universitario de La PrincesaMadridSpain
  3. 3.Hospital Son LlatzerPalma de MallorcaSpain
  4. 4.Hospital Universitario de LeónLeonSpain

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