Journal of Cancer Survivorship

, Volume 12, Issue 2, pp 234–245 | Cite as

Impact of chemotherapy-induced neurotoxicities on adult cancer survivors’ symptom burden and quality of life

  • Christine Miaskowski
  • Judy Mastick
  • Steven M. Paul
  • Gary Abrams
  • Steven Cheung
  • Jennifer Henderson Sabes
  • Kord M. Kober
  • Mark Schumacher
  • Yvette P. Conley
  • Kimberly Topp
  • Betty Smoot
  • Grace Mausisa
  • Melissa Mazor
  • Margaret Wallhagen
  • Jon D. Levine
Article

Abstract

Purpose

Limited information is available on the impact of chemotherapy (CTX)-induced neurotoxicity on adult survivors’ symptom experience and quality of life (QOL). Purposes were to describe occurrence of hearing loss and tinnitus and evaluate for differences in phenotypic characteristics and measures of sensation, balance, perceived stress, symptom burden, and QOL between survivors who received neurotoxic CTX and did (i.e., neurotoxicity group) and did not (i.e., no neurotoxicity group) develop neurotoxicity. Neurotoxicity was defined as the presence of chemotherapy-induced neuropathy (CIN), hearing loss, and tinnitus. Survivors in the no neurotoxicity group had none of these conditions.

Methods

Survivors (n = 609) completed questionnaires that evaluated hearing loss, tinnitus, stress, symptoms, and QOL. Objective measures of sensation and balance were evaluated.

Results

Of the 609 survivors evaluated, 68.6% did and 31.4% did not have CIN. Of the survivors without CIN, 42.4% reported either hearing loss and/or tinnitus and 48.1% of the survivors with CIN reported some form of ototoxicity. Compared to the no neurotoxicity group (n = 110), survivors in the neurotoxicity group (n = 85) were older, were less likely to be employed, had a higher comorbidity burden, and a higher symptom burden, higher levels of perceived stress, and poorer QOL (all p < .05).

Conclusions

Findings suggest that CIN, hearing loss, and tinnitus are relatively common conditions in survivors who received neurotoxic CTX.

Implications for cancer survivors

Survivors need to be evaluated for these neurotoxicities and receive appropriate interventions. Referrals to audiologists and physical therapists are warranted to improve survivors’ hearing ability, functional status, and QOL.

Keywords

Chemotherapy Peripheral neuropathy Hearing loss Tinnitus Balance Survivor 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Disclaimer

Its contents are solely the responsibility of the authors and do not necessarily represent the official views of the NIH. Recruitment was facilitated by Dr. Susan Love Research Foundation’s Army of Women® Program.

References

  1. 1.
    Sogaard M, Thomsen RW, Bossen KS, Sorensen HT, Norgaard M. The impact of comorbidity on cancer survival: a review. Clin Epidemiol. 2013;5(Suppl 1):3–29.  https://doi.org/10.2147/CLEP.S47150clep-5-003.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Denlinger CS, Ligibel JA, Are M, Baker KS, Demark-Wahnefried W, Dizon D, et al. Survivorship: screening for cancer and treatment effects, version 2.2014. J Natl Compr Cancer Netw. 2014;12(11):1526–31.CrossRefGoogle Scholar
  3. 3.
    Bellman SC. Monitoring chemotherapy-induced hearing loss in children. Eur J Cancer. 1996;32A(7):1185–8.CrossRefPubMedGoogle Scholar
  4. 4.
    Brock PR, Knight KR, Freyer DR, Campbell KC, Steyger PS, Blakley BW, et al. Platinum-induced ototoxicity in children: a consensus review on mechanisms, predisposition, and protection, including a new International Society of Pediatric Oncology Boston ototoxicity scale. J Clin Oncol. 2012;30(19):2408–17.  https://doi.org/10.1200/JCO.2011.39.1110.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Freyer DR, Sung L, Reaman GH. Prevention of hearing loss in children receiving cisplatin chemotherapy. J Clin Oncol. 2009;27(2):317–8.  https://doi.org/10.1200/JCO.2008.20.1160.CrossRefPubMedGoogle Scholar
  6. 6.
    Landier W. Ototoxicity and cancer therapy. Cancer. 2016;122(11):1647–8.  https://doi.org/10.1002/cncr.29779.CrossRefPubMedGoogle Scholar
  7. 7.
    Biro K, Noszek L, Prekopp P, Nagyivanyi K, Geczi L, Gaudi I, et al. Characteristics and risk factors of cisplatin-induced ototoxicity in testicular cancer patients detected by distortion product otoacoustic emission. Oncology. 2006;70(3):177–84.CrossRefPubMedGoogle Scholar
  8. 8.
    Bokemeyer C, Berger CC, Hartmann JT, Kollmannsberger C, Schmoll HJ, Kuczyk MA, et al. Analysis of risk factors for cisplatin-induced ototoxicity in patients with testicular cancer. Br J Cancer. 1998;77(8):1355–62.  https://doi.org/10.1038/bjc.1998.226.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Oldenburg J, Kraggerud SM, Cvancarova M, Lothe RA, Fossa SD. Cisplatin-induced long-term hearing impairment is associated with specific glutathione s-transferase genotypes in testicular cancer survivors. J Clin Oncol. 2007;25(6):708–14.CrossRefPubMedGoogle Scholar
  10. 10.
    Frisina RD, Wheeler HE, Fossa SD, Kerns SL, Fung C, Sesso HD, et al. Comprehensive audiometric analysis of hearing impairment and tinnitus after cisplatin-based chemotherapy in survivors of adult-onset cancer. J Clin Oncol. 2016;34(23):2712–20.  https://doi.org/10.1200/JCO.2016.66.8822.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Cheraghi S, Nikoofar P, Fadavi P, Bakhshandeh M, Khoie S, Gharehbagh EJ, et al. Short-term cohort study on sensorineural hearing changes in head and neck radiotherapy. Med Oncol. 2015;32(7):646.  https://doi.org/10.1007/s12032-015-0646-3.CrossRefGoogle Scholar
  12. 12.
    Madasu R, Ruckenstein MJ, Leake F, Steere E, Robbins KT. Ototoxic effects of supradose cisplatin with sodium thiosulfate neutralization in patients with head and neck cancer. Arch Otolaryngol Head Neck Surg. 1997;123(9):978–81.  https://doi.org/10.1001/archotol.1997.01900090094014.CrossRefPubMedGoogle Scholar
  13. 13.
    Salvinelli F, Casale M, Vincenzi B, Santini D, Di Peco V, Firrisi L, et al. Bilateral irreversible hearing loss associated with the combination of carboplatin and paclitaxel chemotherapy: a unusual side effect. J Exp Clin Cancer Res. 2003;22(1):155–8.PubMedGoogle Scholar
  14. 14.
    Sarafraz M, Ahmadi K. Paraclinical evaluation of side-effects of Taxanes on auditory system. Acta Otorhinolaryngol Ital. 2008;28(5):239–42.PubMedPubMedCentralGoogle Scholar
  15. 15.
    Ozguroglu M, Sari O, Turna H. Devastating effects of chemotherapy: deafness and acute renal failure in a patient with epithelial ovarian cancer. Int J Gynecol Cancer. 2006;16(Suppl 1):394–6.  https://doi.org/10.1111/j.1525-1438.2006.00214.x.CrossRefPubMedGoogle Scholar
  16. 16.
    Bacon M, James K, Zee B. A comparison of the incidence, duration, and degree of the neurologic toxicities of cisplatin-paclitaxel (PT) and cisplatin-cyclophosphamide (PC). Int J Gynecol Cancer. 2003;13(4):428–34.  https://doi.org/10.1046/j.1525-1438.2003.13320.x.CrossRefPubMedGoogle Scholar
  17. 17.
    Jenkins V, Low R, Mitra S. Hearing sensitivity in women following chemotherapy treatment for breast cancer: results from a pilot study. Breast. 2009;18(5):279–83.  https://doi.org/10.1016/j.breast.2009.07.004.CrossRefPubMedGoogle Scholar
  18. 18.
    Skalleberg J, Solheim O, Fossa SD, Smastuen MC, Osnes T, Gundersen PO, et al. Long-term ototoxicity in women after cisplatin treatment for ovarian germ cell cancer. Gynecol Oncol. 2017;145(1):148–53.  https://doi.org/10.1016/j.ygyno.2017.02.006.CrossRefPubMedGoogle Scholar
  19. 19.
    Baguley D, McFerran D, Hall D. Tinnitus. Lancet. 2013;382(9904):1600–7.  https://doi.org/10.1016/S0140-6736(13)60142-7.CrossRefPubMedGoogle Scholar
  20. 20.
    Travis LB, Fossa SD, Sesso HD, Frisina RD, Herrmann DN, Beard CJ, et al. Chemotherapy-induced peripheral neurotoxicity and ototoxicity: new paradigms for translational genomics. J Natl Cancer Inst. 2014;106(5):dju044.  https://doi.org/10.1093/jnci/dju044.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Johnson AC, Greenwood-Van MB. Stress-induced pain: a target for the development of novel therapeutics. J Pharmacol Exp Ther. 2014;351(2):327–35.  https://doi.org/10.1124/jpet.114.218065.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Betz LT, Muhlberger A, Langguth B, Schecklmann M. Stress reactivity in chronic tinnitus. Sci Rep. 2017;7:41521.  https://doi.org/10.1038/srep41521.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Heinecke K, Weise C, Schwarz K, Rief W. Physiological and psychological stress reactivity in chronic tinnitus. J Behav Med. 2008;31(3):179–88.  https://doi.org/10.1007/s10865-007-9145-0.CrossRefPubMedGoogle Scholar
  24. 24.
    Woda A, Picard P, Dutheil F. Dysfunctional stress responses in chronic pain. Psychoneuroendocrinology. 2016;71:127–35.  https://doi.org/10.1016/j.psyneuen.2016.05.017.CrossRefPubMedGoogle Scholar
  25. 25.
    Thieme K, Turk DC, Gracely RH, Maixner W, Flor H. The relationship among psychological and psychophysiological characteristics of fibromyalgia patients. J Pain. 2015;16(2):186–96.  https://doi.org/10.1016/j.jpain.2014.11.009.CrossRefPubMedGoogle Scholar
  26. 26.
    Ylikoski J, Lehtimaki J, Pirvola U, Makitie A, Aarnisalo A, Hyvarinen P, et al. Non-invasive vagus nerve stimulation reduces sympathetic preponderance in patients with tinnitus. Acta Otolaryngol. 2017;137(4):1–9.  https://doi.org/10.1080/00016489.2016.1269197.CrossRefGoogle Scholar
  27. 27.
    Vanneste S, De Ridder D. Brain areas controlling heart rate variability in tinnitus and tinnitus-related distress. PLoS One. 2013;8(3):e59728.  https://doi.org/10.1371/journal.pone.0059728.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Miaskowski C, Mastick J, Paul SM, Topp K, Smoot B, Abrams G, et al. Chemotherapy-induced neuropathy in cancer survivors. J Pain Symptom Manag. 2017;54(2):204–218.e2.  https://doi.org/10.1016/j.jpainsymman.2016.12.342.CrossRefGoogle Scholar
  29. 29.
    Victor TW, Jensen MP, Gammaitoni AR, Gould EM, White RE, Galer BS. The dimensions of pain quality: factor analysis of the pain quality assessment scale. Clin J Pain. 2008;24(6):550–5.  https://doi.org/10.1097/AJP.0b013e31816b1058.CrossRefPubMedGoogle Scholar
  30. 30.
    Karnofsky D. Performance scale. Factors that influence the therapeutic response in cancer: a comprehensive treatise. New York: Plenum Press; 1977.Google Scholar
  31. 31.
    Karnofsky D, Abelmann WH, Craver LV, Burchenal JH. The use of nitrogen mustards in the palliative treatment of carcinoma. Cancer. 1948;1(4):634–56.  https://doi.org/10.1002/1097-0142(194811)1:4<634::AID-CNCR2820010410>3.0.CO;2-L.CrossRefGoogle Scholar
  32. 32.
    Schnadig ID, Fromme EK, Loprinzi CL, Sloan JA, Mori M, Li H, et al. Patient-physician disagreement regarding performance status is associated with worse survivorship in patients with advanced cancer. Cancer. 2008;113(8):2205–14.  https://doi.org/10.1002/cncr.23856.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Brunner F, Bachmann LM, Weber U, Kessels AG, Perez RS, Marinus J, et al. Complex regional pain syndrome 1—the Swiss cohort study. BMC Musculoskelet Disord. 2008;9(1):92.  https://doi.org/10.1186/1471-2474-9-92.CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Cieza A, Geyh S, Chatterji S, Kostanjsek N, Ustun BT, Stucki G. Identification of candidate categories of the International Classification of Functioning Disability and Health (ICF) for a Generic ICF Core Set based on regression modelling. BMC Med Res Methodol. 2006;6(1):36.  https://doi.org/10.1186/1471–2288–6-36.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Huang HQ, Brady MF, Cella D, Fleming G. Validation and reduction of FACT/GOG-Ntx subscale for platinum/paclitaxel-induced neurologic symptoms: a gynecologic oncology group study. Int J Gynecol Cancer. 2007;17(2):387–93.CrossRefPubMedGoogle Scholar
  36. 36.
    Bell-Krotoski JA. Sensibility testing with Semmes-Weinstein monofilaments. In: Hunter JM, Mackin EJ, Callahan ED, editors. Rehabilitation of the hand and upper extremity. 5th ed. St. Louis: Mosby, Inc.; 2002.Google Scholar
  37. 37.
    Viswanathan V, Snehalatha C, Seena R, Ramachandran A. Early recognition of diabetic neuropathy: evaluation of a simple outpatient procedure using thermal perception. Postgrad Med J. 2002;78(923):541–2.  https://doi.org/10.1136/pmj.78.923.541.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Papanas N, Ziegler D. New diagnostic tests for diabetic distal symmetric polyneuropathy. J Diabetes Complicat. 2011;25(1):44–51.  https://doi.org/10.1016/j.jdiacomp.2009.09.006.CrossRefPubMedGoogle Scholar
  39. 39.
    Duke J, McEvoy M, Sibbritt D, Guest M, Smith W, Attia J. Vibrotactile threshold measurement for detecting peripheral neuropathy: defining variability and a normal range for clinical and research use. Diabetologia. 2007;50(11):2305–12.  https://doi.org/10.1007/s00125-007-0813-y.CrossRefPubMedGoogle Scholar
  40. 40.
    Tofthagen CS, McMillan SC, Kip KE. Development and psychometric evaluation of the chemotherapy-induced peripheral neuropathy assessment tool. Cancer Nurs. 2011;34(4):E10–20.  https://doi.org/10.1097/NCC.0b013e31820251de.CrossRefPubMedGoogle Scholar
  41. 41.
    Mathias S, Nayak US, Isaacs B. Balance in elderly patients: the “get-up and go” test. Arch Phys Med Rehabil. 1986;67(6):387–9.PubMedGoogle Scholar
  42. 42.
    Hernandez D, Rose DJ. Predicting which older adults will or will not fall using the Fullerton Advanced Balance scale. Arch Phys Med Rehabil. 2008;89(12):2309–15.  https://doi.org/10.1016/j.apmr.2008.05.020.CrossRefPubMedGoogle Scholar
  43. 43.
    Rose DJ, Lucchese N, Wiersma LD. Development of a multidimensional balance scale for use with functionally independent older adults. Arch Phys Med Rehabil. 2006;87(11):1478–85.  https://doi.org/10.1016/j.apmr.2006.07.263.CrossRefPubMedGoogle Scholar
  44. 44.
    Spielberger CG, Gorsuch RL, Suchene R, Vagg PR, Jacobs GA. Manual for the state-anxiety (form Y): self evaluation questionnaire. Palo Alto: Consulting Psychologists Press; 1983.Google Scholar
  45. 45.
    Radloff LS. The CES-D scale: a self-report depression scale for research in the general population. Appl Psychol Meas. 1977;1(3):385–401.  https://doi.org/10.1177/014662167700100306.CrossRefGoogle Scholar
  46. 46.
    Lee KA, Hicks G, Nino-Murcia G. Validity and reliability of a scale to assess fatigue. Psychiatry Res. 1991;36(3):291–8.  https://doi.org/10.1016/0165-1781(91)90027-M.CrossRefPubMedGoogle Scholar
  47. 47.
    Lee KA. Self-reported sleep disturbances in employed women. Sleep. 1992;15(6):493–8.  https://doi.org/10.1093/sleep/15.6.493.CrossRefPubMedGoogle Scholar
  48. 48.
    Cimprich B, Visovatti M, Ronis DL. The attentional function index—a self-report cognitive measure. Psychooncology. 2011;20(2):194–202.  https://doi.org/10.1002/pon.1729.CrossRefPubMedGoogle Scholar
  49. 49.
    Fletcher BS, Paul SM, Dodd MJ, Schumacher K, West C, Cooper B, et al. Prevalence, severity, and impact of symptoms on female family caregivers of patients at the initiation of radiation therapy for prostate cancer. J Clin Oncol. 2008;26(4):599–605.  https://doi.org/10.1200/JCO.2007.12.2838.CrossRefPubMedGoogle Scholar
  50. 50.
    Miaskowski C, Lee KA. Pain, fatigue, and sleep disturbances in oncology outpatients receiving radiation therapy for bone metastasis: a pilot study. J Pain Symptom Manag. 1999;17(5):320–32.  https://doi.org/10.1016/S0885-3924(99)00008-1.CrossRefGoogle Scholar
  51. 51.
    Cimprich B, So H, Ronis DL, Trask C. Pre-treatment factors related to cognitive functioning in women newly diagnosed with breast cancer. Psychooncology. 2005;14(1):70–8.  https://doi.org/10.1002/pon.821.CrossRefPubMedGoogle Scholar
  52. 52.
    Cohen S, Kamarck T, Mermelstein R. A global measure of perceived stress. J Health Soc Behav. 1983;24(4):385–96.  https://doi.org/10.2307/2136404.CrossRefPubMedGoogle Scholar
  53. 53.
    Horowitz M, Wilner N, Alvarez W. Impact of event scale: a measure of subjective stress. Psychosom Med. 1979;41(3):209–18.  https://doi.org/10.1097/00006842-197905000-00004.CrossRefPubMedGoogle Scholar
  54. 54.
    Weiss DS, Marmar CR. The Impact of Event Scale-Revised. Impact of Event Scale-Revised. New York: Guilford Press; 1997.Google Scholar
  55. 55.
    Cuevas BT, Hughes DC, Parma DL, Trevino-Whitaker RA, Ghosh S, Li R, et al. Motivation, exercise, and stress in breast cancer survivors. Support Care Cancer. 2014;22(4):911–7.  https://doi.org/10.1007/s00520-013-2038-6.CrossRefPubMedGoogle Scholar
  56. 56.
    Creamer M, Bell R, Failla S. Psychometric properties of the Impact of Event Scale-Revised. Behav Res Ther. 2003;41(12):1489–96.  https://doi.org/10.1016/j.brat.2003.07.010.CrossRefPubMedGoogle Scholar
  57. 57.
    Civilotti C, Castelli L, Binaschi L, Cussino M, Tesio V, Di Fini G, et al. Dissociative symptomatology in cancer patients. Front Psychol. 2015;6:118.  https://doi.org/10.3389/fpsyg.2015.00118.CrossRefPubMedPubMedCentralGoogle Scholar
  58. 58.
    Sundin EC, Horowitz MJ. Impact of Event Scale: psychometric properties. Br J Psychiatry. 2002;180(3):205–9.  https://doi.org/10.1192/bjp.180.3.205.CrossRefPubMedGoogle Scholar
  59. 59.
    Ware J Jr, Kosinski M, Keller SD. A 12-item short-form health survey: construction of scales and preliminary tests of reliability and validity. Med Care. 1996;34(3):220–33.  https://doi.org/10.1097/00005650-199603000-00003.CrossRefPubMedGoogle Scholar
  60. 60.
    Padilla GV, Ferrell B, Grant MM, Rhiner M. Defining the content domain of quality of life for cancer patients with pain. Cancer Nurs. 1990;13(2):108–15.CrossRefPubMedGoogle Scholar
  61. 61.
    Padilla GV, Presant C, Grant MM, Metter G, Lipsett J, Heide F. Quality of life index for patients with cancer. Res Nurs Health. 1983;6(3):117–26.  https://doi.org/10.1002/nur.4770060305.CrossRefPubMedGoogle Scholar
  62. 62.
    Ferrell BR, Dow KH, Grant M. Measurement of the quality of life in cancer survivors. Qual Life Res. 1995;4(6):523–31.  https://doi.org/10.1007/BF00634747.CrossRefPubMedGoogle Scholar
  63. 63.
    Ferrell BR. The impact of pain on quality of life. A decade of research. Nurs Clin N Am. 1995;30(4):609–24.Google Scholar
  64. 64.
    SPSS. IBM SPSS for windows (version 23). Armonk: SPSS, Inc.; 2015.Google Scholar
  65. 65.
    Bainbridge KE, Wallhagen MI. Hearing loss in an aging American population: extent, impact, and management. Annu Rev Public Health. 2014;35(1):139–52.  https://doi.org/10.1146/annurev-publhealth-032013-182510.CrossRefPubMedGoogle Scholar
  66. 66.
    Hsu WT, Hsu CC, Wen MH, Lin HC, Tsai HT, Su P, et al. Increased risk of depression in patients with acquired sensory hearing loss: a 12-year follow-up study. Medicine. 2016;95(44):e5312.  https://doi.org/10.1097/md.0000000000005312.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Holgers KM, Erlandsson SI, Barrenas ML. Predictive factors for the severity of tinnitus. Audiology. 2000;39(5):284–91.  https://doi.org/10.3109/00206090009073093.CrossRefPubMedGoogle Scholar
  68. 68.
    Pattyn T, Van Den Eede F, Vanneste S, Cassiers L, Veltman DJ, Van De Heyning P, et al. Tinnitus and anxiety disorders: a review. Hear Res. 2016;333:255–65.  https://doi.org/10.1016/j.heares.2015.08.014.CrossRefPubMedGoogle Scholar
  69. 69.
    Tseng CC, Hu LY, Liu ME, Yang AC, Shen CC, Tsai SJ. Risk of depressive disorders following sudden sensorineural hearing loss: a nationwide population-based retrospective cohort study. J Affect Disord. 2016;197:94–9.  https://doi.org/10.1016/j.jad.2016.03.020.CrossRefPubMedGoogle Scholar
  70. 70.
    Gewandter JS, Fan L, Magnuson A, Mustian K, Peppone L, Heckler C, et al. Falls and functional impairments in cancer survivors with chemotherapy-induced peripheral neuropathy (CIPN): a University of Rochester CCOP study. Support Care Cancer. 2013;21(7):2059–66.  https://doi.org/10.1007/s00520-013-1766-y.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Xiao C, Miller AH, Felger J, Mister D, Liu T, Torres MA. Depressive symptoms and inflammation are independent risk factors of fatigue in breast cancer survivors. Psychol Med. 2017;47(10):1–11.  https://doi.org/10.1017/s0033291717000150.CrossRefGoogle Scholar
  72. 72.
    Penedo FJ, Benedict C, Zhou ES, Rasheed M, Traeger L, Kava BR, et al. Association of stress management skills and perceived stress with physical and emotional well-being among advanced prostrate cancer survivors following androgen deprivation treatment. J Clin Psychol Med Settings. 2013;20(1):25–32.  https://doi.org/10.1007/s10880-012-9308-1.CrossRefPubMedGoogle Scholar
  73. 73.
    Mayer DK, Nasso SF, Earp JA. Defining cancer survivors, their needs, and perspectives on survivorship health care in the USA. Lancet Oncol. 2017;18(1):e11–e8.  https://doi.org/10.1016/s1470-2045(16)30573-3.CrossRefPubMedGoogle Scholar
  74. 74.
    Mols F, Vingerhoets AJ, Coebergh JW, van de Poll-Franse LV. Quality of life among long-term breast cancer survivors: a systematic review. Eur J Cancer. 2005;41(17):2613–9.  https://doi.org/10.1016/j.ejca.2005.05.017.CrossRefPubMedGoogle Scholar
  75. 75.
    Jacobs LA, Shulman LN. Follow-up care of cancer survivors: challenges and solutions. Lancet Oncol. 2017;18(1):e19–29.  https://doi.org/10.1016/s1470-2045(16)30386-2.CrossRefPubMedGoogle Scholar
  76. 76.
    Sloan JA, Frost MH, Berzon R, Dueck A, Guyatt G, Moinpour C, et al. The clinical significance of quality of life assessments in oncology: a summary for clinicians. Support Care Cancer. 2006;14(10):988–98.  https://doi.org/10.1007/s00520-006-0085-y.CrossRefPubMedGoogle Scholar
  77. 77.
    Osoba D. Interpreting the meaningfulness of changes in health-related quality of life scores: lessons from studies in adults. Int J Cancer Suppl. 1999;12(S12):132–7.  https://doi.org/10.1002/(SICI)1097-0215(1999)83:12+<132::AID-IJC23>3.0.CO;2-4.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Christine Miaskowski
    • 1
  • Judy Mastick
    • 1
  • Steven M. Paul
    • 1
  • Gary Abrams
    • 2
  • Steven Cheung
    • 2
  • Jennifer Henderson Sabes
    • 2
  • Kord M. Kober
    • 1
  • Mark Schumacher
    • 2
  • Yvette P. Conley
    • 3
  • Kimberly Topp
    • 2
  • Betty Smoot
    • 2
  • Grace Mausisa
    • 1
  • Melissa Mazor
    • 1
  • Margaret Wallhagen
    • 1
  • Jon D. Levine
    • 2
  1. 1.School of NursingUniversity of CaliforniaSan FranciscoUSA
  2. 2.Schools of MedicineUniversity of CaliforniaSan FranciscoUSA
  3. 3.School of NursingUniversity of PittsburghPittsburghUSA

Personalised recommendations