Long term effects of manual lymphatic drainage and active exercises on physical morbidities, lymphoscintigraphy parameters and lymphedema formation in patients operated due to breast cancer: A clinical trial

Mariana Maia Freire de Oliveira, Maria Salete Costa Gurgel, Bárbara Juarez Amorim, Celso Dario Ramos, Sophie Derchain, Natachie Furlan-Santos, César Cabello Dos Santos, Luís Otávio Sarian, Mariana Maia Freire de Oliveira, Maria Salete Costa Gurgel, Bárbara Juarez Amorim, Celso Dario Ramos, Sophie Derchain, Natachie Furlan-Santos, César Cabello Dos Santos, Luís Otávio Sarian

Abstract

Purpose: evaluate whether manual lymphatic drainage (MLD) or active exercise (AE) is associated with shoulder range of motion (ROM), wound complication and changes in the lymphatic parameters after breast cancer (BC) surgery and whether these parameters have an association with lymphedema formation in the long run.

Methods: Clinical trial with 106 women undergoing radical BC surgery, in the Women's Integrated Healthcare Center-University of Campinas. Women were matched for staging, age and body mass index and were allocated to performed AE or MLD, 2 weekly sessions during one month after surgery. The wound was evaluated 2 months after surgery. ROM, upper limb circumference measurement and upper limb lymphoscintigraphy were performed before surgery, and 2 and 30 months after surgery.

Results: The incidence of seroma, dehiscence and infection did not differ between groups. Both groups showed ROM deficit of flexion and abduction in the second month postoperative and partial recovery after 30 months. Cumulative incidence of lymphedema was 23.8% and did not differ between groups (p = 0.29). Concerning the lymphoscintigraphy parameters, there was a significant convergent trend between baseline degree uptake (p = 0.003) and velocity visualization of axillary lymph nodes (p = 0.001) with lymphedema formation. A reduced marker uptake before or after surgery predicted lymphedema formation in the long run (>2 years). None of the lymphoscintigraphy parameters were shown to be associated with the study group. Age ≤39 years was the factor with the greatest association with lymphedema (p = 0.009). In women with age ≤39 years, BMI >24Kg/m2 was significantly associated with lymphedema (p = 0.017). In women over 39 years old, women treated with MLD were at a significantly higher risk of developing lymphedema (p = 0.011).

Conclusion: Lymphatic abnormalities precede lymphedema formation in BC patients. In younger women, obesity seems to be the major player in lymphedema development and, in older women, improving muscle strength through AE can prevent lymphedema. In essence, MLD is as safe and effective as AE in rehabilitation after breast cancer surgery.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1. Flowchart of study sample.
Fig 1. Flowchart of study sample.
Fig 2. Mean shoulder flexion (2A) and…
Fig 2. Mean shoulder flexion (2A) and abduction (2B) at the preoperative of surgery, two and thirty months later, according to group.
Fig 3. Recursive partitioning showing the factors…
Fig 3. Recursive partitioning showing the factors associated with the presence of lymphedema after 30 months of follow-up.

References

    1. DeSantis CE, Lin CC, Mariotto AB, Siegel RL, Stein KD, Kramer JL, et al. Cancer treatment and survivorship statistics, 2014 CA Cancer J Clin. 2014; 64(4): 252–71. doi:
    1. Disipio T, Rye S, Newman B, Hayes S. Incidence of unilateral arm lymphedema after breast cancer: a systematic review and meta-analysis. The Lancet Oncology. 2013;14(6): 500–515. doi:
    1. Sato F, Kuroda Y. Subjective perception of post-operative functional impairment of the arm and its association with quality of life in breast cancer survivors within the first postoperative year. J. Jpn. Acad. Nurs. Sci. 2008; 28, 28–36.
    1. De Groef A, Kampen MV, Dieltjens E, Christiaens MR, Neven P, Geraerts I, Devoogdt N. Effectiveness of postoperative physical therapy for upper-limb impairments after breast cancer treatment: a systematic review. Arch Phys Med Rehabil. 2015;96(6):1140–53.
    1. Shahpar H, Atieh A, Maryam A, Fatemeh HS, Massoome N, Mandana E, et al. Risk Factors of Lymph Edema in Breast Cancer Patients. International Journal of Breast Cancer. 2013. doi:
    1. Fu MR. Breast cancer-related lymphedema: Symptoms, diagnosis, risk reduction, and management. World J Clin Oncol. 2014; 5(3): 241–247 doi:
    1. Testa A, Iannace C, Di Libero L. Strengths of early physical rehabilitation programs in surgical BC patients: results PF a randomized controlled study. Eur J Phys Rehabil Med. 2014; 50: 275–84
    1. Nielsen I, Gordon S, Selby A. Breast cancer-related lymphoedema risk reduction advice: reduction advice: a challenge for health professionals. Cancer Treat Rev. 2008;34(7):621–8. doi:
    1. Celebioglu F, Perbeck L, Frisell J, Grondal E, Svensson L, Danielsson R. Lymph Drainage Studied by Lymphoscintigraphy in the Arms after Sentinel Node Biopsy Compared with Axillary Lymph Node Dissection Following Conservative BC Surgery. Acta Radiologica. 2007; 48(5):488–95. doi:
    1. Shah C, Vicini FA. Breast cancer-related arm lymphedema: incidence rates, diagnostic techniques, optimal management and risk reduction strategies. Int. J. Radiation Oncology Biol. Phys. 2011; 81(4): 907–914.
    1. de Oliveira MM, de Rezende LF, do Amaral MT, Pinto e Silva MP, Morais SS, Gurgel MS. Manual lymphatic drainage versus exercise in the early postoperative period for breast cancer. Physiother Theory Pract. 2014; 30 doi:
    1. Galantino ML, Stout NL. Exercise interventions for upper limb dysfunction due to breast cancer treatment. Phys Ther. 2013;93(10):1291–7. doi:
    1. Scaffidi M, Vulpiani MC, Vetrano M, Conforti F, Marchetti MR, Bonifacino A, et al. Early rehabilitation reduces the onset of complications in the upper limb following breast cancer surgery. Eur J Phys Rehabil Med. 2012; 48(4):601–11.
    1. Gashev AA, Zawieja DC. Physiology of human lymphatic contractility: a historical perspective. Lymphology 2001; 34:124–34.
    1. Schmitz KH, Ahmed RL, Troxel AB, Cheville A, Lewis-Grant L, Smith R, et al. Weight lifting for women at risk for breast cancer-related lymphedema: a randomized trial. JAMA. 2010; 304 doi:
    1. Cheville A. Prevention of lymphoedema after axillary surgery for BC. BMJ. 2010; 340:b5235 doi:
    1. Sarri AJ, Moriguchi SM, Dias R, Peres SV, DA Silva ET, Koga KH, et al. Physiotherapeutic stimulation: Early prevention of lymphedema following axillary lymph node dissection for BC treatment. Experimental and Therapeutic Medicine. 2010; 1: 147–52. doi:
    1. Williams AF, Vadgama A, Franks PJ, Mortimer PS. A randomized controlled crossover study of manual lymphatic drainage therapy in women with BC related lymphedema. European Journal of Cancer Care. 2002; 11: 254–261.
    1. Devoogdt N, Christiaens MR, Geraerts I, Truijen S, Smeets A, Leunen K, et al. Effect of manual lymph drainage in addition to guidelines and exercise therapy on arm lymphoedema related to breast cancer: randomised controlled trial. BMJ. 2011; 343:d5326 doi:
    1. Lacomba MT, Sanches MJY, Goni AZ, Prieto Merino D, Mayoral del Moral O, Cerezo Téllez E, et al. Effectiveness of early physiotherapy to prevent lymphoedema after surgery for breast cancer: randomised, single blinded, clinical Trial. BMJ. 2010; 340:396.
    1. Armer J, Fu MR. Age differences in post-breast cancer lymphedema signs and symptoms. Cancer Nurs. 2005; 28:200–7.
    1. Bains SK, Stanton AWB, Cintolesi V, Ballinger J, Allen S, Zammit C et al. A constitutional predisposition to breast cancer-related lymphoedema and effect of axillary lymph node surgery on forearm muscle lymph flow. The Breast. 2015; 24: 68–74 doi:
    1. Rezende LF, Pedras FV, Ramos CD, Gurgel MSC. Evaluation of lymphatic compensation by lymphoscintigraphy in the postoperative period of breast cancer surgery with axillary dissection. Tumori. 2011; 97: 309–15.
    1. O’Mahony S, Britton TM, Solanki CK, et al. Lymphatic transfer studies with immunoglobulin scintigraphy after axillary surgery. Eur J Surg Oncol. 2007; 33:1052–1060. doi:
    1. Devoogdt N, Van den Wyngaert T, Bourgeois P, Lambrechts M, Van Kampen M, Groef AD, Geraerts I et al. Reproducibility of Lymphoscintigraphic Evaluation of the Upper Limb. Lymphatic Research and Biology. 2014; 12(3). doi:
    1. Lane KN, Dolan LB, Worsley D, McKenzie DC. Upper extremity lymphatic function at rest and during exercise in breast cancer survivors with and without lymphedema compared with healthy controls. J Appl Physiol. 2007;103:917–925. doi:
    1. Modi S, Stanton AW, Svensson WE, Peters AM, Mortimer PS, Levick JR. Human lymphatic pumping measured in healthy and lymphedematous arms by lymphatic congestion lymphoscintigraphy. J Physiol. 2007; 583:271–285. doi:
    1. Stanton AW, Modi S, Mellor RH, Levick JR, Mortimer PS. Recent advances in breast cancer-related lymphedema of the arm: Lymphatic pump failure and predisposing factors. Lymphatic Research Biology. 2009; 7:29–45. doi:
    1. Ferrandez JC, Laroche JP, Serin D, Felix-Faure C, Vinot JM. Lymphoscintigraphic aspects of the effects of manual lymphatic drainage]. J Mal Vasc. 1996; 21:283–289.
    1. Oliveira MMF, Gurgel MSC, Amaral MTP, Amorim BJ, Ramos CD, Almeida Filho JG, Rezende LF, Sarian LOZ. Manual lymphatic drainage and active exercises effects on lymphatic function do not translate into morbidities in women who underwent breast cancer surgery. Accepted to publication on Archives of Physical Medicine and Rehabilitation. 2016
    1. Damstra RJ, Voesten HG, van Schelven WD, van der Lei B. Lymphatic venous anastomosis (LVA) for treatment of secondary arm lymphedema. A prospective study of 11 LVA procedures in 10 patients with breast cancer related lymphedema and a critical review of the literature. Breast Cancer Res Treat. 2009; 113:199–206. doi:
    1. Hothorn T, Hornik K, Zeileis A. Unbiased Recursive Partitioning: A Conditional Inference Framework.Journal of Computational and Graphical Statistics. 2006; 15, Iss. 3
    1. McNeely ML, Campbell K, Ospina M, Rowe BH, Dabbs K, Klassen TP, et al. Exercise interventions for upper-limb dysfunction due to breast cancer treatment. Cochrane Database Syst Rev. 2010;16(6):CD005211.
    1. Karki A, Simonen R, Malkia E, Selfe J. Efficacy of physical therapy methods and exercise after a breast cancer operation: a systematic review. Critical Reviews in Physical and Rehabilitation Medicine. 2001;13(2):159–190.
    1. Shamley DR, Barker K, Simonite V, Beardshaw A. Delayed versus Immediate Exercises following Surgery for Breast Cancer: a systematic review. Breast Cancer Res Treat. 2005;90(3):263–71. doi:
    1. Stuiver MM, ten Tusscher MR, Agasi-Idenburg CS, Lucas C, Aaronson NK, Bossuyt PMM. Conservative interventions for preventing clinically detectable upper-limb lymphoedema in patients who are at risk of developing lymphoedema after breast cancer therapy. Cochrane Database of Systematic Reviews. 2015; 2 Art. No.: CD009765. doi:
    1. Cinar M, Seckin U, Keskin D, Bodur H, Bozkurt B, Cengiz O. The effectiveness of early rehabilitation in patients with modified radical mastectomy. Cancer Nurs. 2008;31(2):160–5.
    1. Do Nascimento SL, de Oliveira RR, de Oliveira MMF, do Amaral MTP. Complicações e condutas fisioterapêuticas após cirurgia por câncer de mama: estudo retrospectivo. Fisioter Pesq. 2012;19(3):248–255.
    1. Levy EW, Pfalzer L, Danoff J, Springer BA, McGarvey C, Shieh CY, et al. Predictors of functional shoulder recovery at 1 and 12 months after breast cancer surgery. Breast Cancer Res Treat. 2012;134(1):315–24. doi:
    1. Zimmermann A, Wozniewski M, Szklarska A, Lipowicz A, Szuba A. Efficacy of manual lymphatic drainage in preventing secondary lymphedema after breast cancer surgery. Lymphology. 2012; 45(3):103–12.
    1. Tartaglione G, Pagan M, Morese R, Cappellini GA, Zappalà AR, Sebastiani C, et al. Intradermal lymphoscintigraphy at rest and after exercise: a new technique for the functional assessment of the lymphatic system in patients with lymphoedema. Nucl Med Commun. 2010; 31(6):547–51.
    1. McGeown JG, McHale NG, Thornbury KD. The role of external compression and movement in lymph propulsion in the sheep hind limb. J Physiol.1987; 387(1):83–93. .
    1. Lane K, Worsley D, Mckenzie D. Exercise and the lymphatic system: implications for breast-cancer survivors. Sport Med. 2005; 35(6):461–71.
    1. Clark B, Sitzia J, Harlow W. Incidence and risk of arm oedema following treatment for breast cancer: a three-year follow-up study. QJM. 2005; 98(5):343–8. .
    1. Zhang L, Fan A, Yan Jun, He Y, Zhang H, Zhang H et al. Combining Manual Lymph Drainage with Physical Exercise after Modified Radical Mastectomy Effectively Prevents Upper Limb Lymphedema. Lymphatic Research and Biology. 2016; 14(2): 104–108. doi:
    1. Togawa K, Ma H, Sullivan-Halley J, Neuhouser ML, Imayama I, Baumgartner KB, et al. Risk factors for self-reported arm lymphedema among reported arm lymphedema among female breast cancer survivors: a prospective cohort study. Breast Cancer Res. 2014;16(4):414 doi:
    1. Kiel K, Rademacker AW. Early-stage breast cancer: arm edema after wide excision and breast irradiation. Radiology 1996;198:279–83 doi:
    1. Meeske KA, Sullivan-Halley J, Smith AW, McTiernan A, Baumgartner KB, Harlan LC, et al. Risk factors for arm lymphedema following breast cancer diagnosis in Black women and White women. Breast Cancer Research and Treatment. 2009; 113(2): 383–391. doi:
    1. Weitman ES, Aschen SZ, Farias-Eisner G, Albano N, Cuzzone DA, Ghanta S, et al. Obesity impairs lymphatic fluid transport and dendritic cell migration to lymph nodes. PLOS ONE. 2013;8(8):e70703 doi:
    1. Greene, Grant FD, Slavin SA, Maclellan RA. Obesity-Induced Lymphedema: Clinical and Lymphoscintigraphic Features. 2015; 35.
    1. Savetsky IL, Torrisi JS, Cuzzone DA, Ghanta S, Albano NJ, Gardenier JC, et al. Obesity increases inflammation and impairs lymphatic function in a mouse model of lymphedema. Am J Physiol Heart Circ Physiol. 2014; 307 doi:
    1. Monleon S, Murta-Nascimento C, Bascuas I, Macià F, Duarte E, Belmonte R. Lymphedema Predictor Factors Factors after BC Surgery: A Survival Analysis. Lymphat Res Biol. 2014; 16 doi:
    1. Cintolesi V, Stanton AWB, Bains SK, Cousins E, Peters AM, Purushotham AD, et al. Constitutively Enhanced Lymphatic Pumping in the Upper Limbs of Women Who Later Develop Breast Cancer-Related Lymphedema. Lymphatic Research and Biology. 2016; 14 doi:
    1. Bae H, Kim HJ. Clinical Outcomes of Extracorporeal Shock Wave Therapy in Patients With Secondary Lymphedema: A Pilot Study. Ann Rehabil Med 2013;37(2):229–234 doi:
    1. Taradaj J, Halski T, Rosinczuk J, Dymarek R, Laurowski A, Smykla A. The influence of Kinesiology Taping on the volume of lymphoedema and manual dexterity of the upper limb in women after breast cancer treatment. European Journal of Cancer Care 2016; 25: 647–660 doi:
    1. E Lima MT, E Lima JG, de Andrade MF, Bergmann A. Low-level laser therapy in secondary lymphedema after breast cancer: systematic review. Lasers Med Sci. 2014; 29(3):1289–95. doi:

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