Advertisement

Breast Cancer Research and Treatment

, Volume 156, Issue 3, pp 453–464 | Cite as

Randomized sham-controlled pilot trial of weekly electro-acupuncture for the prevention of taxane-induced peripheral neuropathy in women with early stage breast cancer

  • Heather Greenlee
  • Katherine D. Crew
  • Jillian Capodice
  • Danielle Awad
  • Donna Buono
  • Zaixing Shi
  • Anne Jeffres
  • Sharon Wyse
  • Wendy Whitman
  • Meghna S. Trivedi
  • Kevin Kalinsky
  • Dawn L. Hershman
Clinical trial

Abstract

To investigate the effect of electro-acupuncture (EA) as a non-pharmacological intervention to prevent or reduce chemotherapy-induced peripheral neuropathy (CIPN) in breast cancer patients undergoing chemotherapy of taxane. Women with stage I-III breast cancer scheduled to receive taxane therapy were randomized to receive a standardized protocol of 12 true or sham EA (SEA) weekly treatments concurrent with taxane treatment. Subjects completed the Brief Pain Inventory-Short Form (BPI-SF), Functional Assessment of Cancer Therapy-Taxane neurotoxicity subscale (FACT-NTX), and other assessments at baseline and weeks 6, 12, and 16. A total of 180 subjects were screened, 63 enrolled and 48 completed week 16 assessments. Mean age was 50 with 25 % white, 25 % black, and 43 % Hispanic; 52 % had no prior chemotherapy. At week 12, both groups reported an increase in mean BPI-SF worst pain score, but no mean differences were found between groups (SEA 2.8 vs. EA 2.6, P = .86). By week 16, the SEA group returned to baseline, while the EA group continued to worsen (SEA 1.7 vs. EA 3.4, P = .03). The increase in BPI-SF worst pain score was 1.62 points higher in the EA group than in the SEA group at week 16 (P = .04). In a randomized, sham-controlled trial of EA for prevention of taxane-induced CIPN, there were no differences in pain or neuropathy between groups at week 12. Of concern, subjects on EA had a slower recovery than SEA subjects. Future studies should focus on EA for treatment as opposed to prevention of CIPN.

Keywords

Acupuncture Electro-acupuncture Breast cancer Chemotherapy-induced peripheral neuropathy Taxane 

Notes

Research Support

Breast Cancer Research Foundation (to DLH), National Cancer Institute NCI K23CA141052 (to HG).

Compliance with ethical standards

Ethical standards

The experiments performed in this study comply with all relevant laws in the United States. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

10549_2016_3759_MOESM1_ESM.docx (1 mb)
Supplementary material 1 (DOCX 1035 kb)

References

  1. 1.
    Cavaletti G, Zanna C (2002) Current status and future prospects for the treatment of chemotherapy-induced peripheral neurotoxicity. Eur J Cancer 38:1832–1837. doi: 10.1016/S0959-8049(02)00229-0 CrossRefPubMedGoogle Scholar
  2. 2.
    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(3):767–774. doi: 10.1007/s10549-010-1278-0 CrossRefPubMedGoogle Scholar
  3. 3.
    Speck RM, Samuel 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
  4. 4.
    Carlson K, Ocean AJ (2011) Peripheral neuropathy with microtubule-targeting agents: occurrence and management approach. Clin Breast Cancer 11(2):73–81. doi: 10.1016/j.clbc.2011.03.006 CrossRefPubMedGoogle Scholar
  5. 5.
    Havrilesky LJ, Reiner M, Morrow PK, Watson H, Crawford J (2015) A review of relative dose intensity and survival in patients with metastatic solid tumors. Crit Rev Oncol 93(3):203–210. doi: 10.1016/j.critrevonc.2014.10.006 CrossRefGoogle Scholar
  6. 6.
    Henderson IC, Berry DA, Demetri GD, Cirrincione CT, Goldstein LJ, Martino S, Ingle JN, Cooper MR, Hayes DF, Tkaczuk KH, Fleming G, Holland JF, Duggan DB, Carpenter JT, Frei E, Schilsky RL, Wood WC, Muss HB, Norton L (2003) Improved outcomes from adding sequential paclitaxel but not from escalating doxorubicin dose in an adjuvant chemotherapy regimen for patients with node-positive primary breast cancer. J Clin Oncol 21:976–983. doi: 10.1200/JCO.2003.02.063 CrossRefPubMedGoogle Scholar
  7. 7.
    Martin M, Ruiz A, Ruiz Borrego M, Barnadas A, Gonzalez S, Calvo L, Margeli Vila M, Anton A, Rodriguez-Lescure A, Segui-Palmer MA, Munoz-Mateu M, Dorca Ribugent J, Lopez-Vega JM, Jara C, Espinosa E, Mendiola Fernandez C, Andres R, Ribelles N, Plazaola A, Sanchez-Rovira P, Salvador Bofill J, Crespo C, Carabantes FJ, Servitja S, Chacon JI, Rodriguez CA, Hernando B, Alvarez I, Carrasco E, Lluch A (2013) Fluorouracil, doxorubicin, and cyclophosphamide (FAC) versus FAC followed by weekly paclitaxel as adjuvant therapy for high-risk, node-negative breast cancer: results from the GEICAM/2003-02 study. J Clin Oncol 31(20):2593–2599. doi: 10.1200/JCO.2012.46.9841 CrossRefPubMedGoogle Scholar
  8. 8.
    Martin M, Segui MA, Anton A, Ruiz A, Ramos M, Adrover E, Aranda I, Rodriguez-Lescure A, Grosse R, Calvo L, Barnadas A, Isla D, Martinez del Prado P, Ruiz Borrego M, Zaluski J, Arcusa A, Munoz M, Lopez Vega JM, Mel JR, Munarriz B, Llorca C, Jara C, Alba E, Florian J, Li J, Lopez Garcia-Asenjo JA, Saez A, Rios MJ, Almenar S, Peiro G, Lluch A, Investigators G (2010) Adjuvant docetaxel for high-risk, node-negative breast cancer. N Engl J Med 363(23):2200–2210. doi: 10.1056/NEJMoa0910320 CrossRefPubMedGoogle Scholar
  9. 9.
    Sparano JA, Wang M, Martino S, Jones V, Perez EA, Saphner T, Wolff AC, Sledge GW, Wood WC, Davidson NE (2008) Weekly paclitaxel in the adjuvant treatment of breast cancer. N Engl J Med 358:1663–1671. doi: 10.1056/NEJMoa0707056 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    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 CrossRefPubMedGoogle Scholar
  11. 11.
    Smith EM, Pang H, Cirrincione C, Fleishman S, Paskett ED, Ahles T, Bressler LR, Fadul CE, Knox C, Le-Lindqwister N, Gilman PB, Shapiro CL, Alliance for Clinical Trials in O (2013) Effect of duloxetine on pain, function, and quality of life among patients with chemotherapy-induced painful peripheral neuropathy: a randomized clinical trial. JAMA 309(13):1359–1367. doi: 10.1001/jama.2013.2813 CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Hershman DL, Lacchetti C, Dworkin RH, Lavoie Smith EM, Bleeker J, Cavaletti G, Chauhan C, Gavin P, Lavino A, Lustberg MB, Paice J, Schneider B, Smith ML, Smith T, Terstriep S, Wagner-Johnston N, Bak K, Loprinzi CL (2014) Prevention and management of chemotherapy- induced peripheral neuropathy in survivors of adult cancers: American society of clinical oncology clinical practice guideline. J Clin Oncol 32:1941–1967. doi: 10.1200/JCO.2013.54.0914 CrossRefPubMedGoogle Scholar
  13. 13.
    Hammack JE, Michalak JC, Loprinzi CL, Sloan JA, Novotny PJ, Soori GS, Tirona MT, Rowland KM, Stella PJ, Johnson JA (2002) Phase III evaluation of nortriptyline for alleviation of symptoms of cis-platinum-induced peripheral neuropathy. Pain 98:195–203. doi: 10.1016/S0304-3959(02)00047-7 CrossRefPubMedGoogle Scholar
  14. 14.
    Kautio AL, Haanpaa M, Saarto T, Kalso E (2008) Amitriptyline in the treatment of chemotherapy-induced neuropathic symptoms. J Pain Symptom Manag 35(1):31–39. doi: 10.1016/j.jpainsymman.2007.02.043 CrossRefGoogle Scholar
  15. 15.
    Rao RD, Flynn PJ, Sloan JA, Wong GY, Novotny P, Johnson DB, Gross HM, Renno SI, Nashawaty M, Loprinzi CL (2008) Efficacy of lamotrigine in the management of chemotherapy-induced peripheral neuropathy: a phase 3 randomized, double-blind, placebo-controlled trial, N01C3. Cancer 112(12):2802–2808. doi: 10.1002/cncr.23482 CrossRefPubMedGoogle Scholar
  16. 16.
    Rao RD, Michalak JC, Sloan JA, Loprinzi CL, Soori GS, Nikcevich DA, Warner DO, Novotny P, Kutteh LA, Wong GY, North Central Cancer Treatment G (2007) Efficacy of gabapentin in the management of chemotherapy-induced peripheral neuropathy: a phase 3 randomized, double-blind, placebo-controlled, crossover trial (N00C3). Cancer 110(9):2110–2118. doi: 10.1002/cncr.23008 CrossRefPubMedGoogle Scholar
  17. 17.
    Barton DL, Wos EJ, Qin R, Mattar BI, Green NB, Lanier KS, Bearden JD 3rd, Kugler JW, Hoff KL, Reddy PS, Rowland KM Jr, Riepl M, Christensen B, Loprinzi CL (2011) A double-blind, placebo-controlled trial of a topical treatment for chemotherapy-induced peripheral neuropathy: NCCTG trial N06CA. Support Care Cancer: Off J Multinatl Assoc Support Care Cancer 19(6):833–841. doi: 10.1007/s00520-010-0911-0 CrossRefGoogle Scholar
  18. 18.
    MacPherson H, Thomas K, Walters S, Fitter M (2001) The York acupuncture safety study: prospective survey of 34 000 treatments by traditional acupuncturists. BMJ 323:486–487. doi: 10.1136/bmj.323.7311.486 CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Han JS (2004) Acupuncture and endorphins. Neurosci Lett 361(1–3):258–261. doi: 10.1016/j.neulet.2003.12.019 CrossRefPubMedGoogle Scholar
  20. 20.
    Paley CA, Johnson MI, Tashani OA, Bagnall A-M (2011) Acupuncture for cancer pain in adults. Cochrane Database Syst Rev. doi: 10.1002/14651858.CD007753.pub2 PubMedGoogle Scholar
  21. 21.
    Bennett MI, Johnson MI, Brown SR, Radford H, Brown JM, Searle RD (2010) Feasibility study of transcutaneous electrical nerve stimulation (TENS) for cancer bone pain. J Pain: Off J Am Pain Soc 11(4):351–359. doi: 10.1016/j.jpain.2009.08.002 CrossRefGoogle Scholar
  22. 22.
    Brami C, Bao T, Deng G (2016) Natural products and complementary therapies for chemotherapy-induced peripheral neuropathy: a systematic review. Crit Rev Oncol Hematol 98:325–334. doi: 10.1016/j.critrevonc.2015.11.014 CrossRefPubMedGoogle Scholar
  23. 23.
    Keller S, Bann CM, Dodd SL, Schein J, Mendoza TR, Cleeland CS (2004) Validity of the brief pain inventory for use in documenting the outcomes of patients with noncancer pain. Clin J Pain 20:309–318. doi: 10.1097/00002508-200409000-00005 CrossRefPubMedGoogle Scholar
  24. 24.
    Cella D, Peterman A, Hudgens S, Webster K, Socinski MA (2003) Measuring the side effects of taxane therapy in oncology: the Functional Assessment of Cancer Therapy-Taxane (FACT-Taxane). Cancer 98:822–831. doi: 10.1002/cncr.11578 CrossRefPubMedGoogle Scholar
  25. 25.
    Galer BS, Jensen MP (1997) Development and preliminary validation of a pain measure specific to neuropathic pain: the neuropathic pain scale. Neurology 48:332–338. doi: 10.1212/WNL.48.2.332 CrossRefPubMedGoogle Scholar
  26. 26.
    Bloom S, Till S, Sonksen P, Smith S (1984) Use of a biothesiometer to measure individual vibration thresholds and their variation in 519 non-diabetic subjects. BMJ 288:1793–1795. doi: 10.1136/bmj.288.6433.1793 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Ruff RM, Parker SB (1993) Gender- and age-specific changes in motor speed and eye-hand coordination in adults: normative values for the finger tapping and grooved pegboard tests. Percept Mot Skills 76:1219–1230. doi: 10.2466/pms.1993.76.3c.1219 CrossRefPubMedGoogle Scholar
  28. 28.
    Park J, White A, Lee H, Ernst E (1999) Development of a new sham needle. Acupunct Med 17(2):110–112. doi: 10.1136/aim.17.2.110 CrossRefGoogle Scholar
  29. 29.
    Wong R, Sagar S (2006) Acupuncture treatment for chemotherapy-induced peripheral neuropathy—a case series. Acupunct Med 24:87–91. doi: 10.1136/aim.24.2.87 CrossRefPubMedGoogle Scholar
  30. 30.
    Bao T, Zhang R, Badros A, Lao L (2011) Acupuncture treatment for bortezomib-induced peripheral neuropathy: a case report. Pain Res Treat 2011:920807. doi: 10.1155/2011/920807 PubMedPubMedCentralGoogle Scholar
  31. 31.
    Schroeder S, Meyer-Hamme G, Epplée S (2012) Acupuncture for chemotherapy-induced peripheral neuropathy (CIPN): a pilot study using neurography. Acupunct Med 30:4–7. doi: 10.1136/acupmed-2011-010034 CrossRefPubMedGoogle Scholar
  32. 32.
    Donald GK, Tobin I, Stringer J (2011) Evaluation of acupuncture in the management of chemotherapy-induced peripheral neuropathy. Acupunct Med 29:230–233. doi: 10.1136/acupmed.2011.010025 CrossRefPubMedGoogle Scholar
  33. 33.
    Bao T, Goloubeva O, Pelser C, Porter N, Primrose J, Hester L, Sadowska M, Lapidus R, Medeiros M, Lao L, Dorsey SG, Badros AZ (2014) A pilot study of acupuncture in treating bortezomib-induced peripheral neuropathy in patients with multiple myeloma. Integr Cancer Ther 13:396–404. doi: 10.1177/1534735414534729 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Xu W-R, Hua B-J, Hou W, Bao Y-J (2010) Clinical randomized controlled study on acupuncture for treatment of peripheral neuropathy induced by chemotherapeutic drugs. Zhongguo Zhen Jiu 30:457–460PubMedGoogle Scholar
  35. 35.
    Lu W, Matulonis UA, Dunn JE, Lee H, Doherty-Gilman A, Dean-Clower E, Goodman A, Davis RB, Buring J, Wayne P, Rosenthal DS, Penson RT (2012) The feasibility and effects of acupuncture on quality of life scores during chemotherapy in ovarian cancer: results from a pilot, randomized sham-controlled trial. Acupunct Med 24:233–240. doi: 10.1089/acu.2012.0904 CrossRefGoogle Scholar
  36. 36.
    Chen H, Liu T-Y, Kuai L, Zhu J, Wu C-J, Liu L-M (2013) Electroacupuncture treatment for pancreatic cancer pain: a randomized controlled trial. Pancreatol: Off J Int Assoc Pancreatol (IAP) [et al] 13:594–597. doi: 10.1016/j.pan.2013.10.007 CrossRefGoogle Scholar
  37. 37.
    Dharmananda S (2002) Electro-acupuncture. Subhuti Dharmananda. http://www.itmonline.org/arts/electro.htm. Accessed 4 March 2016
  38. 38.
    Bauml J, Xie SX, Farrar JT, Bowman MA, Li SQ, Bruner D, DeMichele A, Mao JJ (2014) Expectancy in real and sham electroacupuncture: does believing make it so? J Natl Cancer Inst Monogr 2014:302–307. doi: 10.1093/jncimonographs/lgu029 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Lin CC, Chen MC, Yu SN, Ju MS (2005) Chronic electrical stimulation of four acupuncture points on rat diabetic neuropathy. In: Conference proceedings: annual international conference of the IEEE Engineering in Medicine and Biology Society IEEE engineering in medicine and biology society annual conference, vol 4, pp 4271–4274. doi: 10.1109/iembs.2005.1615408
  40. 40.
    Schroder S, Liepert J, Remppis A, Greten JH (2007) Acupuncture treatment improves nerve conduction in peripheral neuropathy. Eur J Neurol 14(3):276–281. doi: 10.1111/j.1468-1331.2006.01632.x PubMedGoogle Scholar
  41. 41.
    Abuaisha BB, Costanzi JB, Boulton AJ (1998) Acupuncture for the treatment of chronic painful peripheral diabetic neuropathy: a long-term study. Diabetes Res Clin Pract 39(2):115–121. doi: 10.1016/S0168-8227(97)00123-X CrossRefPubMedGoogle Scholar
  42. 42.
    Zijlstra FJ, van den Berg-de LI, Huygen FJ, Klein J (2003) Anti-inflammatory actions of acupuncture. Mediat Inflamm 12(2):59–69. doi: 10.1080/0962935031000114943 CrossRefGoogle Scholar
  43. 43.
    Arrieta Ó, Hernández-Pedro N, Fernández-González-Aragón MC, Saavedra-Pérez D, Campos-Parra AD, Ríos-Trejo MÁ, Cerón-Lizárraga T, Martínez-Barrera L, Pineda B, Ordóñez G, Ortiz-Plata A, Granados-Soto V, Sotelo J (2011) Retinoic acid reduces chemotherapy-induced neuropathy in an animal model and patients with lung cancer. Neurology 77:987–995. doi: 10.1212/WNL.0b013e31822e045c CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Heather Greenlee
    • 1
    • 2
    • 5
  • Katherine D. Crew
    • 1
    • 2
    • 3
  • Jillian Capodice
    • 4
  • Danielle Awad
    • 2
    • 3
  • Donna Buono
    • 1
  • Zaixing Shi
    • 1
  • Anne Jeffres
    • 2
  • Sharon Wyse
    • 2
  • Wendy Whitman
    • 2
  • Meghna S. Trivedi
    • 3
  • Kevin Kalinsky
    • 2
    • 3
  • Dawn L. Hershman
    • 1
    • 2
    • 3
  1. 1.Mailman School of Public HealthColumbia UniversityNew YorkUSA
  2. 2.Herbert Irving Comprehensive Cancer CenterColumbia UniversityNew YorkUSA
  3. 3.College of Physicians and SurgeonsColumbia UniversityNew YorkUSA
  4. 4.Mount Sinai School of MedicineNew YorkUSA
  5. 5.Columbia UniversityNew YorkUSA

Personalised recommendations