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Breast Cancer Research and Treatment

, Volume 142, Issue 1, pp 109–118 | Cite as

Risk of docetaxel-induced peripheral neuropathy among 1,725 Danish patients with early stage breast cancer

  • L. Eckhoff
  • A. S. Knoop
  • M.-B. Jensen
  • B. Ejlertsen
  • M. Ewertz
Clinical trial

Abstract

Docetaxel-induced peripheral neuropathy (PN) can lead to sub-optimal treatment in women with early breast cancer. Here, we compare the frequency of dose reduction as a result of PN in two different adjuvant regimens. From the Danish Breast Cancer Cooperative Group READ trial we included 1,725 patients with early stage breast cancer who randomly were assigned to three cycles of epirubicin and cyclophosphamide followed by three cycles docetaxel (D100) or six cycles of cyclophosphamide and docetaxel (D75). Eligible patients completed chemotherapy, received docetaxel, and provided information on patient-reported outcome (secondary outcome of trial) including PN. Associations between PN and risk factors were analyzed by multivariate logistic regression. Overall 597 patients (34 %) reported PN, grades 2–4, during treatment, 194 (11 %) after the first cycle [early onset peripheral neuropathy (EPN)] and 403 (23 %) after subsequent cycles [later-onset peripheral neuropathy (LPN)]. The odds ratio (OR) of EPN was significantly increased for the D100 regimen (OR 3.10; 95 % CI 2.18–4.42) while this regimen was associated with reduced OR of LPN (OR 0.69; 95 % CI 0.54–0.88). Patients with PN received significantly lower cumulative doses of docetaxel than patients with no PN. Explorative analysis showed that OR of PN was significantly reduced if patients wore frozen gloves and socks during treatment (OR 0.56; 95 % CI 0.38–0.81) in the EPN group. Patients developing PN after the first cycle are less likely to receive docetaxel at the planned dose intensity and usage of frozen gloves and socks may modify the risk.

Keywords

Breast cancer Docetaxel Chemotherapy-induced peripheral neuropathy Dose reduction 

Notes

Acknowledgments

The READ trial/Danish Breast Cancer Cooperative Group received an unrestricted grant from Sanofis-aventis.

Conflict of interest

Bent Ejlertsen MD, has received unrestricted grants from Norvatis, Amgen, and Roche. All other authors have no conflict of interest.

References

  1. 1.
  2. 2.
    Akerley W, Herndon JE, Egorin MJ, Lyss AP, Kindler HL, Savarese DM, Sherman CA, Rosen DM, Hollis D, Ratain MJ, Green MR (2003) Weekly, high-dose paclitaxel in advanced lung carcinoma: a phase II study with pharmacokinetics by the Cancer and Leukemia Group B. Cancer 97:2480–2486. doi: 10.1002/cncr.11375 PubMedCrossRefGoogle Scholar
  3. 3.
    Argyriou AA, Bruna J, Marmiroli P, Cavaletti G (2012) Chemotherapy-induced peripheral neurotoxicity (CIPN): an update. Crit Rev Oncol/Hematol 82:51–77. doi: 10.1016/j.critrevonc.2011.04.012 CrossRefGoogle Scholar
  4. 4.
    Argyriou AA, Polychronopoulos P, Koutras A, Iconomou G, Gourzis P, Assimakopoulos K, Kalofonos HP, Chroni E (2006) Is advanced age associated with increased incidence and severity of chemotherapy-induced peripheral neuropathy? Supportive care in cancer: official journal of the Multinational Association of Supportive Care in Cancer 14:223–229. doi: 10.1007/s00520-005-0868-6 CrossRefGoogle Scholar
  5. 5.
    Bakitas MA (2007) Background noise: the experience of chemotherapy-induced peripheral neuropathy. Nurs Res 56:323–331. doi: 10.1097/01.NNR.0000289503.22414.79 PubMedCrossRefGoogle Scholar
  6. 6.
    Basch E, Iasonos A, McDonough T, Barz A, Culkin A, Kris MG, Scher HI, Schrag D (2006) Patient versus clinician symptom reporting using the National Cancer Institute Common Terminology Criteria for Adverse Events: results of a questionnaire-based study. Lancet Oncol 7:903–909. doi: 10.1016/S1470-2045(06)70910-X PubMedCrossRefGoogle Scholar
  7. 7.
    Boehmke MM, Dickerson SS (2005) Symptom, symptom experiences, and symptom distress encountered by women with breast cancer undergoing current treatment modalities. Cancer Nurs 28:382–389PubMedCrossRefGoogle Scholar
  8. 8.
    Bria E, Nistico C, Cuppone F, Carlini P, Ciccarese M, Milella M, Natoli G, Terzoli E, Cognetti F, Giannarelli D (2006) Benefit of taxanes as adjuvant chemotherapy for early breast cancer: pooled analysis of 15,500 patients. Cancer 106:2337–2344. doi: 10.1002/cncr.21886 PubMedCrossRefGoogle Scholar
  9. 9.
    Broyl A, Corthals SL, Jongen JL, van der Holt B, Kuiper R, de Knegt Y, van Duin M, el Jarari L, Bertsch U, Lokhorst HM, Durie BG, Goldschmidt H, Sonneveld P (2010) Mechanisms of peripheral neuropathy associated with bortezomib and vincristine in patients with newly diagnosed multiple myeloma: a prospective analysis of data from the HOVON-65/GMMG-HD4 trial. Lancet Oncol 11:1057–1065. doi: 10.1016/S1470-2045(10)70206-0 PubMedCrossRefGoogle Scholar
  10. 10.
    Can G, Aydiner A, Cavdar I (2012) Taxane-induced nail changes: predictors and efficacy of the use of frozen gloves and socks in the prevention of nail toxicity. Eur J Oncol Nurs 16:270–275. doi: 10.1016/j.ejon.2011.06.007 PubMedCrossRefGoogle Scholar
  11. 11.
    Charlson ME, Pompei P, Ales KL, MacKenzie CR (1987) A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis 40:373–383PubMedCrossRefGoogle Scholar
  12. 12.
    Chaudhry V, Chaudhry M, Crawford TO, Simmons-O’Brien E, Griffin JW (2003) Toxic neuropathy in patients with pre-existing neuropathy. Neurology 60:337–340PubMedCrossRefGoogle Scholar
  13. 13.
    Chaudhry V, Rowinsky EK, Sartorius SE, Donehower RC, Cornblath DR (1994) Peripheral neuropathy from taxol and cisplatin combination chemotherapy: clinical and electrophysiological studies. Ann Neurol 35:304–311. doi: 10.1002/ana.410350310 PubMedCrossRefGoogle Scholar
  14. 14.
    Early Breast Cancer Trialists’ Collaborative G, Peto R, Davies C, Godwin J, Gray R, Pan HC, Clarke M, Cutter D, Darby S, McGale P, Taylor C, Wang YC, Bergh J, Di Leo A, Albain K, Swain S, Piccart M, Pritchard K (2012) Comparisons between different polychemotherapy regimens for early breast cancer: meta-analyses of long-term outcome among 100,000 women in 123 randomised trials. Lancet 379:432–444. doi:  10.1016/S0140-6736(11)61625-5 Google Scholar
  15. 15.
    Eckhoff L, Nielsen M, Moeller S, Knoop A (2011) TAXTOX - a retrospective study regarding the side effects of docetaxel given as part of the adjuvant treatment to patients with primary breast cancer in Denmark from 2007 to 2009. Acta Oncol 50:1075–1082. doi: 10.3109/0284186X.2011.602111 PubMedCrossRefGoogle Scholar
  16. 16.
    Ellis P, Barrett-Lee P, Johnson L, Cameron D, Wardley A, O’Reilly S, Verrill M, Smith I, Yarnold J, Coleman R, Earl H, Canney P, Twelves C, Poole C, Bloomfield D, Hopwood P, Johnston S, Dowsett M, Bartlett JM, Ellis I, Peckitt C, Hall E, Bliss JM (2009) Sequential docetaxel as adjuvant chemotherapy for early breast cancer (TACT): an open-label, phase III, randomised controlled trial. Lancet 373:1681–1692. doi: 10.1016/S0140-6736(09)60740-6 PubMedCrossRefGoogle Scholar
  17. 17.
    Fromme EK, Eilers KM, Mori M, Hsieh YC, Beer TM (2004) How accurate is clinician reporting of chemotherapy adverse effects? A comparison with patient-reported symptoms from the Quality-of-Life Questionnaire C30. J Clin Oncol 22:3485–3490. doi: 10.1200/JCO.2004.03.025 PubMedCrossRefGoogle Scholar
  18. 18.
    Hashimoto N, Yokoyama K, Sadahira K, Ueda T, Tsukada Y, Okamoto S (2012) Itraconazole may increase the risk of early onset bortezomib-induced peripheral neuropathy. Int J Hematol 96:758–763. doi: 10.1007/s12185-012-1224-5 PubMedCrossRefGoogle Scholar
  19. 19.
    Hausheer FH, Schilsky RL, Bain S, Berghorn EJ, Lieberman F (2006) Diagnosis, management, and evaluation of chemotherapy-induced peripheral neuropathy. Semin Oncol 33:15–49. doi: 10.1053/j.seminoncol.2005.12.010 PubMedCrossRefGoogle Scholar
  20. 20.
    Hershman DL, Weimer LH, Wang A, Kranwinkel G, Brafman L, Fuentes D, Awad D, Crew KD (2011) Association between patient reported outcomes and quantitative sensory tests for measuring long-term neurotoxicity in breast cancer survivors treated with adjuvant paclitaxel chemotherapy. Breast Cancer Res Treat 125:767–774. doi: 10.1007/s10549-010-1278-0 PubMedCrossRefGoogle Scholar
  21. 21.
    Hilkens PH, Verweij J, Stoter G, Vecht CJ, van Putten WL, van den Bent MJ (1996) Peripheral neurotoxicity induced by docetaxel. Neurology 46:104–108PubMedCrossRefGoogle Scholar
  22. 22.
    Hilkens PH, Verweij J, Vecht CJ, Stoter G, van den Bent MJ (1997) Clinical characteristics of severe peripheral neuropathy induced by docetaxel (Taxotere). Ann Oncol 8:187–190PubMedCrossRefGoogle Scholar
  23. 23.
    Ishiguro H, Takashima S, Yoshimura K, Yano I, Yamamoto T, Niimi M, Yamashiro H, Ueno T, Takeuchi M, Sugie T, Yanagihara K, Toi M, Fukushima M (2012) Degree of freezing does not affect efficacy of frozen gloves for prevention of docetaxel-induced nail toxicity in breast cancer patients. Support Care Cancer 20:2017–2024. doi: 10.1007/s00520-011-1308-4 PubMedCrossRefGoogle Scholar
  24. 24.
    Jimenez-Andrade JM, Peters CM, Mejia NA, Ghilardi JR, Kuskowski MA, Mantyh PW (2006) Sensory neurons and their supporting cells located in the trigeminal, thoracic and lumbar ganglia differentially express markers of injury following intravenous administration of paclitaxel in the rat. Neurosci Lett 405:62–67. doi: 10.1016/j.neulet.2006.06.043 PubMedCrossRefGoogle Scholar
  25. 25.
    Jones SE, Erban J, Overmoyer B, Budd GT, Hutchins L, Lower E, Laufman L, Sundaram S, Urba WJ, Pritchard KI, Mennel R, Richards D, Olsen S, Meyers ML, Ravdin PM (2005) Randomized phase III study of docetaxel compared with paclitaxel in metastatic breast cancer. J Clin Oncol 23:5542–5551. doi: 10.1200/JCO.2005.02.027 PubMedCrossRefGoogle Scholar
  26. 26.
    Lee JJ, Swain SM (2006) Peripheral neuropathy induced by microtubule-stabilizing agents. J Clin Oncol 24:1633–1642. doi: 10.1200/JCO.2005.04.0543 PubMedCrossRefGoogle Scholar
  27. 27.
    Loprinzi CL, Maddocks-Christianson K, Wolf SL, Rao RD, Dyck PJ, Mantyh P, Dyck PJ (2007) The Paclitaxel acute pain syndrome: sensitization of nociceptors as the putative mechanism. Cancer J 13:399–403. doi: 10.1097/PPO.0b013e31815a999b PubMedCrossRefGoogle Scholar
  28. 28.
    Loprinzi CL, Reeves BN, Dakhil SR, Sloan JA, Wolf SL, Burger KN, Kamal A, Le-Lindqwister NA, Soori GS, Jaslowski AJ, Novotny PJ, Lachance DH (2011) Natural history of paclitaxel-associated acute pain syndrome: prospective cohort study NCCTG N08C1. J Clin 29:1472–1478. doi: 10.1200/JCO.2010.33.0308 CrossRefGoogle Scholar
  29. 29.
    Mir O, Alexandre J, Tran A, Durand JP, Pons G, Treluyer JM, Goldwasser F (2009) Relationship between GSTP1 Ile(105)Val polymorphism and docetaxel-induced peripheral neuropathy: clinical evidence of a role of oxidative stress in taxane toxicity. Ann Oncol 20:736–740. doi: 10.1093/annonc/mdn698 PubMedCrossRefGoogle Scholar
  30. 30.
    New PZ, Jackson CE, Rinaldi D, Burris H, Barohn RJ (1996) Peripheral neuropathy secondary to docetaxel (Taxotere). Neurology 46:108–111PubMedCrossRefGoogle Scholar
  31. 31.
    Peters CM, Jimenez-Andrade JM, Jonas BM, Sevcik MA, Koewler NJ, Ghilardi JR, Wong GY, Mantyh PW (2007) Intravenous paclitaxel administration in the rat induces a peripheral sensory neuropathy characterized by macrophage infiltration and injury to sensory neurons and their supporting cells. Exp Neurol 203:42–54. doi: 10.1016/j.expneurol.2006.07.022 PubMedCrossRefGoogle Scholar
  32. 32.
    Peters CM, Jimenez-Andrade JM, Kuskowski MA, Ghilardi JR, Mantyh PW (2007) An evolving cellular pathology occurs in dorsal root ganglia, peripheral nerve and spinal cord following intravenous administration of paclitaxel in the rat. Brain Res 1168:46–59. doi: 10.1016/j.brainres.2007.06.066 PubMedCrossRefGoogle Scholar
  33. 33.
    Petersen MA, Larsen H, Pedersen L, Sonne N, Groenvold M (2006) Assessing health-related quality of life in palliative care: comparing patient and physician assessments. Eur J Cancer 42:1159–1166. doi: 10.1016/j.ejca.2006.01.032 PubMedCrossRefGoogle Scholar
  34. 34.
    Reeves BN, Dakhil SR, Sloan JA, Wolf SL, Burger KN, Kamal A, Le-Lindqwister NA, Soori GS, Jaslowski AJ, Kelaghan J, Novotny PJ, Lachance DH, Loprinzi CL (2012) Further data supporting that paclitaxel-associated acute pain syndrome is associated with development of peripheral neuropathy: north Central Cancer Treatment Group trial N08C1. Cancer 118:5171–5178. doi: 10.1002/cncr.27489 PubMedCrossRefGoogle Scholar
  35. 35.
    Schloss JM, Colosimo M, Airey C, Masci PP, Linnane AW, Vitetta L (2013) Nutraceuticals and chemotherapy induced peripheral neuropathy (CIPN): A systematic review. Clin Nutr. doi:  10.1016/j.clnu.2013.04.007
  36. 36.
    Schneider BP, Zhao F, Wang M, Stearns V, Martino S, Jones V, Perez EA, Saphner T, Wolff AC, Sledge GW Jr, Wood WC, Davidson NE, Sparano JA (2012) Neuropathy is not associated with clinical outcomes in patients receiving adjuvant taxane-containing therapy for operable breast cancer. J Clin Oncol 30:3051–3057. doi: 10.1200/JCO.2011.39.8446 PubMedCrossRefGoogle Scholar
  37. 37.
    Scotte F, Banu E, Medioni J, Levy E, Ebenezer C, Marsan S, Banu A, Tourani JM, Andrieu JM, Oudard S (2008) Matched case–control phase 2 study to evaluate the use of a frozen sock to prevent docetaxel-induced onycholysis and cutaneous toxicity of the foot. Cancer 112:1625–1631. doi: 10.1002/cncr.23333 PubMedCrossRefGoogle Scholar
  38. 38.
    Scotte F, Tourani JM, Banu E, Peyromaure M, Levy E, Marsan S, Magherini E, Fabre-Guillevin E, Andrieu JM, Oudard S (2005) Multicenter study of a frozen glove to prevent docetaxel-induced onycholysis and cutaneous toxicity of the hand. J Clin Oncol 23:4424–4429. doi: 10.1200/JCO.2005.15.651 PubMedCrossRefGoogle Scholar
  39. 39.
    Shimozuma K, Ohashi Y, Takeuchi A, Aranishi T, Morita S, Kuroi K, Ohsumi S, Makino H, Mukai H, Katsumata N, Sunada Y, Watanabe T, Hausheer FH (2009) Feasibility and validity of the Patient Neurotoxicity Questionnaire during taxane chemotherapy in a phase III randomized trial in patients with breast cancer: N-SAS BC 02. Support Care Cancer 17:1483–1491. doi: 10.1007/s00520-009-0613-7 PubMedCrossRefGoogle Scholar
  40. 40.
    Sissung TM, Baum CE, Deeken J, Price DK, Aragon-Ching J, Steinberg SM, Dahut W, Sparreboom A, Figg WD (2008) ABCB1 genetic variation influences the toxicity and clinical outcome of patients with androgen-independent prostate cancer treated with docetaxel. Clin Cancer Res 14:4543–4549. doi: 10.1158/1078-0432.CCR-07-4230 PubMedCrossRefGoogle Scholar
  41. 41.
    Speck RM, DeMichele A, Farrar JT, Hennessy S, Mao JJ, Stineman MG, Barg FK (2012) Scope of symptoms and self-management strategies for chemotherapy-induced peripheral neuropathy in breast cancer patients. Support Care Cancer 20:2433–2439. doi: 10.1007/s00520-011-1365-8 PubMedCrossRefGoogle Scholar
  42. 42.
    Speck RM, Sammel MD, Farrar JT, Hennessy S, Mao JJ, Stineman MG, Demichele A (2013) Impact of chemotherapy-induced peripheral neuropathy on treatment delivery in nonmetastatic breast cancer. J Oncol Pract. doi: 10.1200/jop.2012.000863 PubMedGoogle Scholar
  43. 43.
    Stubblefield MD, Burstein HJ, Burton AW, Custodio CM, Deng GE, Ho M, Junck L, Morris GS, Paice JA, Tummala S, Von Roenn JH (2009) NCCN task force report: management of neuropathy in cancer. J Natl Compr Cancer Netw: JNCCN 7 Suppl 5:S1–S26; quiz S27–28Google Scholar
  44. 44.
    Sucheston LE, Zhao H, Yao S, Zirpoli G, Liu S, Barlow WE, Moore HC, Thomas Budd G, Hershman DL, Davis W, Ciupak GL, Stewart JA, Isaacs C, Hobday TJ, Salim M, Hortobagyi GN, Gralow JR, Livingston RB, Albain KS, Hayes DF, Ambrosone CB (2011) Genetic predictors of taxane-induced neurotoxicity in a SWOG phase III intergroup adjuvant breast cancer treatment trial (S0221). Breast Cancer Res Treat 130:993–1002. doi:  10.1007/s10549-011-1671-3 Google Scholar
  45. 45.
    Swain SM, Arezzo JC (2008) Neuropathy associated with microtubule inhibitors: diagnosis, incidence, and management. Clin Adv Hematol Oncol 6:455–467PubMedGoogle Scholar
  46. 46.
    Tanabe Y, Hashimoto K, Shimizu C, Hirakawa A, Harano K, Yunokawa M, Yonemori K, Katsumata N, Tamura K, Ando M, Kinoshita T, Fujiwara Y (2013) Paclitaxel-induced peripheral neuropathy in patients receiving adjuvant chemotherapy for breast cancer. Int J Clin Oncol 18:132–138. doi: 10.1007/s10147-011-0352-x PubMedCrossRefGoogle Scholar
  47. 47.
    Winer EP, Berry DA, Woolf S, Duggan D, Kornblith A, Harris LN, Michaelson RA, Kirshner JA, Fleming GF, Perry MC, Graham ML, Sharp SA, Keresztes R, Henderson IC, Hudis C, Muss H, Norton L (2004) Failure of higher-dose paclitaxel to improve outcome in patients with metastatic breast cancer: cancer and leukemia group B trial 9342. J Clin Oncol 22:2061–2068. doi: 10.1200/JCO.2004.08.048 PubMedCrossRefGoogle Scholar
  48. 48.
    Wolf S, Barton D, Kottschade L, Grothey A, Loprinzi C (2008) Chemotherapy-induced peripheral neuropathy: prevention and treatment strategies. Eur J Cancer 44:1507–1515. doi: 10.1016/j.ejca.2008.04.018 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • L. Eckhoff
    • 1
    • 2
  • A. S. Knoop
    • 3
  • M.-B. Jensen
    • 4
  • B. Ejlertsen
    • 3
    • 4
  • M. Ewertz
    • 1
  1. 1.Department of OncologyOdense University HospitalOdenseDenmark
  2. 2.Institute of Clinical ResearchUniversity of Southern DenmarkOdenseDenmark
  3. 3.Department of OncologyRigshospitalet, Copenhagen University HospitalCopenhagenDenmark
  4. 4.Danish Breast Cancer Cooperative GroupRigshospitalet, Copenhagen University HospitalCopenhagenDenmark

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