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Abstract

Lymphedema is a troublesome condition faced by many breast cancer survivors today. Since lymphedema represents a debilitating and progressive problem that is feared by most breast cancer patients and their providers, an up-to-date understanding is necessary in order to better diagnose, treat and manage these patients. The etiology of lymphedema is multifactorial and poorly understood. Although lymphedema is not clearly defined within the medical community, there are several diagnostic tools available to the clinician, of which the most widely accepted in the clinical setting are the arm circumference measurements. Misinformation has recently been conveyed regarding activity recommendations for those patients afflicted with lymphedema. These recent events highlight the critical importance of education, heightened awareness and dedicated future cooperative research in order to favorably impact on lymphedema care and the quality of life for those living with lymphedema.

Keywords

breast cancer compression garment decongestive lymphatic therapy lymphedema

Lymphedema (LE) is a progressive and debilitating condition that is incurable but treatable. It is often under-recognized and mistreated. LE is known to be associated with significant morbidity, both physical and psychological. The majority of cases in western countries comprise secondary or acquired LE, particularly following cancer treatment. Increased risk for this type of LE has been attributed to many factors, such as disease burden, surgery, radiation, infection or trauma. Breast cancer treatment is recognized as the most common cause of secondary LE in developed countries [1]. Early intervention in the care of LE portends the best overall outcome [2].

Given the fact that breast cancer is the most common cancer diagnosed in women worldwide, and that new advanced therapies continue to positively affect survivorship, an increasing number of women will be at risk for developing secondary LE.

Incidence

Breast cancer has consistently remained the leading cancer diagnosis in women, with approximately 192,000 cases having been diagnosed in the USA in 2009 [3]. Over 2.5 million breast cancer survivors are alive in the USA today [3,4], and it is estimated that 12% of women (approximately one in eight) will develop breast cancer in their lifetime [4]. There has been significant variation in the reported incidence rates of breast cancer-related LE, with the current literature citing 6–85% [5 –9]. This variation in reported incidence can probably be explained by the differences in the length of follow-up between studies, the varying methods for diagnosis, the variable surgical/radiation treatments received by the affected women and an inconsistency in the measurement systems employed [7]. If LE incidence is conservatively estimated at 25%, then more than 600,000 breast cancer survivors are currently afflicted with this condition.

It is important to distinguish that breast cancer-related LE can involve the upper extremities as well as the entire truncal region [10], including the breast, chest wall and supraclavicular area. LE of the upper extremities can involve the entire extremity or be limited to specific regions of the extremity, such as the posterior elbow or hand [10].

It is essential to recognize that certain milestones in the study of LE and in the treatment of breast cancer over the past 10 years have resulted in a decrease in the incidence of LE. Regarding surgical therapy, the introduction of sentinel lymph node biopsy (SLNB) in the surgical treatment of breast cancer has significantly reduced the incidence of LE, with reported ranges of LE incidence being between 1 and 17% in those receiving SLNB only, without completion axillary node dissection [11 –16]. SLNB, which is now the standard of care in early-stage breast cancer in developed countries, allows for the removal of substantially fewer lymph nodes compared with axillary lymph node dissection in which, traditionally, all of the lymphatic contents within the level I and level II axillary nodal basin are excised. However, although SLNB reduces the incidence of LE, risk still remains from this procedure and other breast cancer treatment modalities. A new technique emerging in the literature is axillary reverse mapping, which attempts to identify and protect the lymphatics draining the arm during axillary surgery for breast cancer [17]. Long-term follow-up data for the axillary reverse mapping procedure are necessary in order to evaluate whether this technique results in a lower incidence of LE.

The movement toward less aggressive axillary surgery is fostered by the increased awareness that the extent of nodal surgery and the number of nodes removed appear to correlate with arm LE risk. In a study evaluating both arm and breast LE after breast cancer treatment, including surgery and radiation, breast edema was reported to be more common than arm LE (9.6 vs 7.6%, respectively) [18].

Although it is generally agreed upon by both healthcare providers and patients that LE is a highly feared complication of breast cancer therapy, the absolute causes of LE have yet to be identified. This is a possible explanation for the frequent misinformation regarding LE and delay in diagnosis. Risk factors that disrupt the locoregional lymphatics, such as axillary surgery, mastectomy and radiation to the breast and axilla, have been identified [10]. Regarding the development of arm LE, significant variables include the number of nodes removed, the size of the primary tumor and multifield irradiation. For breast edema, increased BMI and the upper outer quadrant tumor site were significant risk factors.

Patients presenting with breast cancer need to receive adequate pretreatment education regarding LE and need to understand that it is a known complication of breast cancer therapies. This full disclosure will promote awareness and increase early detection.

Diagnosing lymphedema

Lymphedema results from dysfunction in lymphatic transport, which causes an abnormal accumulation of proteinrich fluid within the interstitium of the affected area. Subsequently, swelling occurs followed by inflammation, adipose tissue hypertrophy and fibrosis, which can lead to disfigurement of the involved region [19].

Patients may initially report vague symptoms such as fatigue or aching within the arm or breast area, or more ominous sensations of heaviness or swelling. These can often be mistaken or dismissed in the early postoperative period or falsely attributed to multimodality treatment [2]. It is also important to rule out other etiologies for these symptoms, such as cancer recurrence, infection or deep vein thrombosis [18,20]. There has been significant research on the development and validation of subjective symptoms and their relationship to objective measurements for LE. Armer et al. demonstrated, with the use of the Lymphedema and Breast Cancer Questionnaire, that patient self-reported symptoms of ‘heaviness in the past year’ and ‘swelling now’ were predictive of increased upper extremity circumference measurements [21].

Currently, there is neither consensus regarding the quantitative definition of LE, nor is there a uniformly accepted method for the measurement of LE. Historically, the gold standard method for measuring limbs has been water displacement. However, water displacement is not practical in a routine clinical setting, since it is both cumbersome and time-consuming. Recording circumferential limb measurements has been the most widely implemented method for assessing limb changes in clinical practice; however, it is not without significant limitations. Baseline measurements are often not available from which to accurately record change, the anatomic location of the measurement is frequently variable and operator dependent, and the degree of change that represents LE is not accurately defined [1]. The perometer, an optoelectronic volumetry device, uses infrared light and an array of optoelectronic sensors to assess limb volume [1,22]. Perometry has been demonstrated to be reliable and efficient in the clinical setting; however, the perometer device is a costly unit. Bioelectrical impedance spectroscopy measures the tissue opposition (impedance) of body tissues with a low, alternating electric current over a range of frequencies to determine extracellular fluid volume [23]. The magnitude of the impedance is used to determine the extracellular fluid volume and is expressed as an impedance ratio. Tissue tonometry is another method that measures the resistance of tissues to compression and quantifies tissue compliance. The degree of compressibility can then be correlated with limb swelling.

In a prospective study, Armer and Stewart compared four diagnostic criteria for LE in breast cancer patients: 200 ml perometry limb volume change (LVC); 10% perometry LVC; 2 cm circumferential increase; and reports of heaviness or swelling ‘now’ or ‘in the past year’ (subjective symptoms) [6]. Using these four criteria, the incidence of LE was found to be quite variable, from the lowest incidence reported in the 10% LVC group (21%) to the highest incidence reported in the 2 cm circumferential change group (85%) after 24-month follow-up. Interestingly, serial circumferential limb measurements are most commonly utilized for LE assessment, which, according to this study, has the highest reported incidence of LE (Table 1). The variability observed in this study clearly demonstrates a critical need for both a concise definition and a standardized measurement method for LE.

Table 1.

Lymphedema occurrence utilizing different diagnostic criteria.

Diagnostic criteria	6 months (%)	12 months (%)	18 months (%)	24 months (%)
200 ml limb volume change	24	40	49	56
10% limb volume change	9	22	28	34
2 cm difference in limb circumference	45	72	79	85
Signs and symptoms	17	31	35	37

Adapted with permission from [5].

Diagnostic imaging is not commonly used to diagnose LE. At present, no clinically available macroscopic imaging modality has sufficient temporal or spatial resolution to image tumor-induced changes to the lymphatics in vivo, nor do they have the required resolution to image the lymphatic changes associated with the etiology of LE or its response to therapy. However, if imaging is required, lymphoscintigraphy has essentially replaced direct contrast lymphography as the imaging modality of choice for the evaluation of patients with suspected LE. This technique utilizes a radiotracer such as technetium TC 99m-filtered sulfur colloid, which is injected into the dermis of the affected limb [24]. MRI and computed tomography imaging can be used as adjuncts, primarily to rule out primary or recurrent tumors; however, the use of these imaging methodologies adds considerable cost.

Treatment

Poage et al., as part of the Oncology Nursing Society (ONS), presented a Putting Evidence Into Practice® card for LE after an extensive systematic review of the literature [2]. Treatment modalities that primarily focused on volume reduction were stratified into the following categories based on the level of published evidence: ‘effective’, ‘likely to be effective’, ‘benefits balanced with harms’, ‘effectiveness not established’ and ‘not recommended for practice’.

Effective interventions that are recommended for treatment included decongestive lymphatic therapy (DLT), compression bandaging and treatment of infection. Interventions that were deemed ‘likely to be effective’ were maintaining optimal body weight and manual lymph drainage [2,20]. Interventions in which the evidence suggested that there were ‘benefits balanced with harms’ included exercise, prophylactic antibiotics recurrent infections and surgical intervention [2]. Those interventions that are not supported by the current body of literature were categorized as ‘effectiveness not established as single modality treatment’ and included compression garments, hyperbaric oxygen, low-level laser treatment, pneumatic compression pump, simple lymphatic drainage and nanocrystalline silver dressing on lymphatic ulcers [2]. Finally, those treatments ‘not recommended for practice’ were pharmaceutical agents such as diuretics and benzopyrenes [2].

For those patients with breast LE, it is important to note that manual lymphatic drainage (MLD) and compression bandaging in the acute initial period are typically very successful, with significant improvements observed within 2 weeks [10]. Only some patients require intermittent management and follow-up. With arm LE, MLD is also very effective, as discussed later in this article; however, all patients generally require a long-term compression sleeve and follow-up [18].

Decongestive lymphatic therapy consists of an initial reductive phase (phase I) followed by an ongoing individual maintenance phase (phase II) [2,101]. The goals of DLT are to decrease edema, increase lymph drainage from the congested areas, reduce subdermal fibrosis, improve the skin condition, enhance the patient's functional status and enable the patient to adhere to an independent self-care program [25,26,101]. DLT includes MLD, compression bandaging, lymphatic/decongestive exercise, skin care, education in the self-management of LE and elastic compression garments (Box 1) [20,27]. The duration of phase I is typically 2–4 weeks and includes MLD to evacuate the fluid out of the congested areas and compression bandaging to maintain progress between sessions. MLD is recommended daily [25,27]. Phase I treatment should be directed by a qualified professional who is trained in DLT. Upon completion of phase I, the patient should be appropriately fitted with a compression garment. It is important to differentiate compression bandaging from compression garments. Compression bandaging involves multiple layers of short-stretch (non-elastic) bandages that are regularly applied to achieve a desired pressure gradient. A compression garment provides long-term control of LE with compression between 20 and 60 mmHg. Garments need to be replaced at regular intervals in order to maintain their effectiveness [101].

Box 1.

Breast cancer-related lymphedema.

Decongestive lymphatic therapy†: phase I – initial reductive phase; phase II – individualized maintenance phase

MLD:

Specialized hands-on technique designed to direct lymphatic flow out of congested areas into functional nodal basins

Compression bandaging:

– Multiple layers of short-stretch bandages with limited extensibility utilized to achieve a specific compression gradient, creating a pump for congested lymph

Remedial exercise:

– Therapist-directed regimen; compression garments must be worn during exercise in order to counterbalance excessive formation and accumulation of interstitial fluid

Skin care:

– Maintaining excellent hygiene; application of low pH moisturizers

Compression garment:

– Follows phase I; essential for long-term control; wash regularly and replace at regular intervals

LE self-management education:

– Emphasis on lifelong nature of the condition; education on self-MLD, signs/symptoms of cellulitis, fitting and care of compression garments, weight control and individualized LE exercise programs (under the direction of a certified therapist)

Symptom management‡

Cognitive coping:

– Understanding the need for behavioral changes and overcoming obstacles and barriers, supported by education and discussion of factors that improve or exacerbate LE

Psychological coping:

– Setting, meeting and maintaining management goals

Social coping:

– Utilizing support groups

Direct support:

– Direct interaction and education regarding diagnosis and symptoms to ease distress and patient's feeling of abandonment

†

Data from [101].

‡

Data from [30].

LE: Lymphedema; MLD: Manual lymph drainage.

Infection is a serious complication of breast cancer-related LE, contributing significant morbidity and cost to the treatment of LE [28]. Patients can develop acute inflammatory episodes within the affected limb or breast after surgery and/or radiation. The cause of a majority of these episodes is suspected to be streptococci, and penicillin therapy is typically curative. A majority of patients report skin injury as the inciting event. Unfortunately, making the diagnosis of cellulitis in an affected area with LE can be difficult since the classic cellulitis presentation of demarcated erythema is often absent. Prior to definitive treatment of a single episode with antibiotics, rest and elevation, it is important to rule out deep venous thrombosis. In the case of recurrent or severe infection, broader spectrum intravenous antibiotic therapy to include coverage of Staphylococcus may be warranted. After resolution of the acute episode, prophylactic antibiotics should be considered, particularly in populations that develop recurrent infections [29].

Living with lymphedema

Breast cancer-related LE is an abnormal accumulation of lymph in the arm, shoulder, breast or thoracic area that typically develops within 36 months of treatment but can develop at any time [30]. This accumulation of fluid causes discomfort and pain, impaired function and emotional distress. Quality of life has been demonstrated to be significantly lowered in patients with breast cancer-related LE. Physical symptoms that appear to be statistically significant to quality of life are alterations in limb sensation, decreased physical activity and fatigue [31].

Adhering to the often rigorous and demanding treatment regimens is difficult and relentless. Studies have identified that breast cancer survivors with LE have more difficulties with anxiety, depression and relationships [30]. Fu et al. explored breast cancer survivors' experiences with breast cancer-related LE and reported the following themes: living with perpetual discomfort, confronting the unexpected, losing pre-LE being and feeling handicapped [32]. Further research is needed to address the psychosocial aspects of breast cancer-related LE. Furthermore, the cost of breast cancer-related LE in a study by Shih et al. reported on LE patients with medical costs between US$14,877 and US$23,167 higher than matched controls [28].

The successful management of LE involves treatment delivery by qualified professionals as well as life-long diligent self-care. Healthcare provider and patient education are vital to successful early diagnosis, intervention and longterm management. In a recent study, Fu et al. reported that patients who received information on breast cancer-related LE had significantly fewer symptoms [33]. The National Lymphedema Network (NLN) has issued a series of position papers on the controversial and important aspects of LE to address the needs of providers and patients, such as treatment guidelines, risk reduction measures, air travel and exercise, in order to dispel myths and false information [102].

Reducing risk of infection & increased swelling

The LE patient's understanding and proactive approach to risk reduction is crucial. Meticulous skin care to avoid infection includes using daily moisturizers, noninvasive nail care, the use of sunscreen/insect repellent, razor precaution, utilizing gloves in order to avoid trauma and obtaining early treatment for signs/symptoms of infection [103]. Patients should wear loose-fitting jewelry and clothing and, if possible, offer the nonaffected extremity for blood draws or blood pressure [103]. The compression garment should be appropriately well-fitted and utilized for any strenuous activity. Prolonged exposure to cold and heat should be avoided [103].

Air travel

Regarding air travel, patients with LE are often misdirected since there is conflicting evidence in the literature concerning whether air travel has the potential to cause or exacerbate LE. The following air travel precautions are agreed upon by a majority of LE specialists [34,104]: patients with a known diagnosis of LE should wear some form of compression sleeve with a glove before take-off and for several hours after deplaning in order to reduce the risk of swelling; those who are at risk for LE should discuss their risk/benefit profile of wearing a compression garment with their healthcare provider. Other precautions for the traveler with LE or who are at risk for LE include regular movement of the extremities, maintaining hydration and avoiding direct handling of heavy luggage [104].

Exercise

Lymphatic remedial exercise is a widely accepted beneficial and integral component of DLT [27]. In addition, mobility exercise is a known component of rehabilitation for breast cancer patients in the postoperative period. Recently, exercise in LE patients has been a focus of controversy [35]. As with many aspects of LE, the term ‘exercise’ has been used erroneously. Patients as well as healthcare providers involved in the treatment of LE have been historically fearful of resistance exercise. Therefore, the exercise dilemma is specifically centered on resistive training for those afflicted with LE.

In 2006, two prospective randomized clinical trials evaluated the effect of supervised exercise regimes in breast cancer patients after axillary lymph node dissection. Ahmed et al. reported on the LE data from the Weight Training for Breast Cancer Survivors (WTBS) study. Both trials concluded that supervised forms of exercise did not increase the risk, nor did they worsen the symptoms of LE [36,37]. In 2009, Schmitz et al. reported the results of a larger prospective clinical trial with 141 breast cancer survivors with stable LE who were randomized to either a directly supervised and regulated weight lifting program or a control group [38]. Their study results demonstrated that slow progressive weight lifting under stringent criteria to include the use of a full compression garment did not have a significant effect on limb swelling and improved overall function and quality of life.

Prior to initiating any supervised weight lifting program, for which only patients with stable LE should be considered, the patient should be familiar with the risk reduction recommendations, possess a solid understanding of LE and treatment and agree to seek care from a qualified LE specialist should symptoms arise or exacerbation develop. In addition, the exercise program should be initiated in a controlled fashion and be slowly progressive. Proper execution of exercise is key to avoiding injury. At present, no evidence-based recommendations can be made regarding resistive exercise programs for those patients who are at risk of, but have not yet developed, LE.

Future perspective

Lymphedema is a growing health problem that significantly impacts the life of many breast cancer survivors. Education and increased awareness within our healthcare system is vital from the time of diagnosis through to long-term follow-up. Referral to appropriately certified therapists for evaluation and treatment should be the standard of care for breast cancer patients with suspected or confirmed LE.

With healthcare reform imminent, immediate action is needed to improve the following: recognition of LE as a diagnosis, access to treatment and insurance coverage for the necessary treatment. Without standardized diagnostic criteria and measurement tools, the current data will remain both complex and confusing. Cooperative research in the form of large multicenter, prospective, randomized, controlled trials with standardized guidelines is needed, so that results can impact all aspects of LE care and effect change. By resolving the conflicting recommendations for breast cancer patients with LE, progress regarding this debilitating condition can finally be accomplished.

Executive summary

Epidemiology

Breast cancer consistently remains the leading cancer diagnosed in women, with over 2.5 million breast cancer survivors in the USA today.

The reported incidence of breast cancer-related lymphedema is widely variable (between 6 and 85%) owing to the lack of defined diagnostic criteria and inconsistent measurement protocols, as well as variable treatments and follow-up.

Breast cancer-related lymphedema can involve the trunk, ipsilateral breast and chest wall, as well as the upper extremities.

Sentinel lymph node biopsy is associated with a lower incidence of lymphedema compared with axillary lymph node dissection.

Axillary reverse mapping is an investigational technique that could potentially protect the lymphatics draining the arm during routine axillary surgery for breast cancer.

Patient-reported symptoms of ‘heaviness in the past year’ or ‘swelling now’ are predictive of increased upper extremity circumference measurements that are consistent with lymphedema.

Specific causal relationships among risk factors for lymphedema have not yet been identified.

Education regarding this formidable complication prior to any breast cancer treatments is required for patients.

Diagnosing lymphedema

Initial patient-reported symptoms are often mistaken or dismissed when patients are undergoing breast cancer treatment.

No consensus regarding a quantitative definition of lymphedema currently exists.

There is no widely accepted reliable measurement metric for the diagnosis and follow-up of lymphedema.

Available measurement methods include water displacement (the gold standard), circumferential limb measurements, perometry, bioimpedance spectroscopy and tonometry.

Treatment

Decongestive lymphatic therapy, including manual lymph drainage, compression bandaging, lymphatic exercises, skin care, patient education regarding self-management and elastic compression garments, is currently the international standard of care for the treatment of lymphedema.

Various treatment efforts have been evaluated and categorized by the level of evidence for recommendation in practice. This is available from the Oncology Nursing Society as Putting Evidence Into Practice®.

Breast lymphedema tends to respond more rapidly to acute treatment, whereas upper extremity lymphedema often requires long-term use of compression garments.

Infection is a serious complication of lymphedema, requiring prompt intervention.

Living with lymphedema

General life-long risk reduction practices should include diligent skin care, avoidance of trauma/injury, appropriate utilization of compression garments that include hand coverage and avoidance of prolonged exposure to cold and heat.

Management of both the physical and emotional symptoms is important in the comprehensive, multidisciplinary treatment of lymphedema.

It is recommended that patients with lymphedema wear compression garments during air travel.

Supervised lymphatic decongestive exercises and mobility rehabilitation are recognized forms of exercise treatment for breast cancer patients with lymphedema.

Resistive exercise is currently a focus of interest. Patients with diagnosed stable lymphedema may consider a resistive exercise program under direct supervision with the involvement of appropriately certified lymphedema therapists. This should take place with correct compression garment application and successful education and awareness regarding the symptoms of lymphedema exacerbation.

Future perspective

Healthcare reform needs to address lymphedema as a recognized condition that requires access to and insurance coverage for necessary treatment.

Multicenter, prospective, randomized controlled clinical trials are necessary in order to standardize diagnostic criteria and measurement methods that will provide the results that are necessary to definitively improve lymphedema care.

Footnotes

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties.

No writing assistance was utilized in the production of this manuscript.

References

Papers of special note have been highlighted as:

of interest

of considerable interest

Armer

: The problem of post-breast cancer lymphedema: impact and measurement issues. Cancer Invest. 23(1), 76–83 (2005).

Poage

Singer

Armer

Poundall

Shellabarger

: Demystifying lymphedema: development of the lymphedema putting evidence into practice card. Clin. J. Oncol. Nurs. 12(6), 951–964 (2008).

Important reference providing evidence in support of current practice.

Horner

Ries

Krapcho

: SEER Cancer Statistics Review 1975–2006. National Cancer Institute, MD, USA (2009).

American Cancer Society: Cancer Facts and Figures – 2009. American Cancer Society, GA, USA (2010).

Armer

Stewart

Shook

: 30-month post-breast cancer treatment lymphedema. J. Lymphoedema 4(1), 14–18 (2009).

10.

Important paper in the field of breast cancer-related lymphedema.

11.

Armer

Stewart

: A comparison of four diagnostic criteria for lymphedema in a post-breast cancer population. Lymphat. Res. Biol. 3(4), 208–217 (2005).

12.

Important paper regarding lymphedema evaluation.

13.

Petrek

Heelan

: Incidence of breast carcinoma-related lymphedema. Cancer 83(12 Suppl. American), 2776–2781 (1998).

14.

Ahmed

Prizment

Lazovich

Schmitz

Folsom

: Lymphedema and quality of life in breast cancer survivors: the Iowa Women's Health Study. J. Clin. Oncol. 26(35), 5689–5696 (2008).

15.

Petrek

Senie

Peters

Rosen

: Lymphedema in a cohort of breast carcinoma survivors 20 years after diagnosis. Cancer 92(6), 1368–1377 (2001).

16.

Muscari

: Lymphedema: responding to our patients' needs. Oncol. Nurs. Forum 31(5), 905–912 (2004).

17.

Blanchard

Donohue

Reynolds

Grant

: Relapse and morbidity in patients undergoing sentinel lymph node biopsy alone or with axillary dissection for breast cancer. Arch. Surg. 138(5), 482–487; discussion 487–488 (2003).

18.

Francis

Abghari

Rymal

Suna

Kosir

: Improving surgical outcomes: standardizing the reporting of incidence and severity of acute lymphedema after sentinel lymph node biopsy and axillary lymph node dissection. Am. J. Surg. 192(5), 636–639 (2006).

19.

Langer

Guller

Berclaz

: Morbidity of sentinel lymph node biopsy (SLN) alone versus SLN and completion axillary lymph node dissection after breast cancer surgery: a prospective swiss multicenter study on 659 patients. Ann. Surg. 245(3), 452–461 (2007).

20.

Mansel

Fallowfield

Kissin

: Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC trial. J. Natl Cancer Inst. 98(9), 599–609 (2006).

21.

Landmark paper of historical importance.

22.

Schijven

Vingerhoets

Rutten

: Comparison of morbidity between axillary lymph node dissection and sentinel node biopsy. Eur. J. Surg. Oncol. 29(4), 341–350 (2003).

23.

Wilke

Mccall

Posther

: Surgical complications associated with sentinel lymph node biopsy: results from a prospective international cooperative group trial. Ann. Surg. Oncol 13(4), 491–500 (2006).

24.

Landmark paper of historical importance.

25.

Boneti

Korourian

Diaz

: Scientific impact award: axillary reverse mapping (ARM) to identify and protect lymphatics draining the arm during axillary lymphadenectomy. Am. J. Surg. 198(4), 482–487 (2009).

26.

Goffman

Laronga

Wilson

Elkins

: Lymphedema of the arm and breast in irradiated breast cancer patients: risks in an era of dramatically changing axillary surgery. Breast J. 10(5), 405–411 (2004).

27.

Warren

Brorson

Borud

Slavin

: Lymphedema: a comprehensive review. Ann. Plast. Surg. 59(4), 464–472 (2007).

28.

Rockson

Miller

Senie

: American cancer society lymphedema workshop. Workgroup III: diagnosis and management of lymphedema. Cancer 83(12 Suppl. American), 2882–2885 (1998).

29.

Armer

Radina

Porock

Culbertson

: Predicting breast cancer-related lymphedema using self-reported symptoms. Nurs. Res. 52(6), 370–379 (2003).

30.

Petlund

: Volumetry of Limbs. CRC Press, MA, USA 444–451 (1991).

31.

Ward

: Is BIS ready for prime time as the gold standard measure? J. Lymphoedema 4(2), 52–56 (2009).

32.

Witte

: Diagnostic and interventional imaging of lymphatic disorders. Int. Angiol. 18(1), 25–30 (1999).

33.

Ferrandez

Laroche

Serin

Felix-Faure

Vinot

: Lymphoscintigraphic aspects of the effects of manual lymphatic drainage. J. Mal. Vasc. 21(5), 283–289 (1996).

34.

Weiss

Spray

: The effect of complete decongestive therapy on the quality of life of patients with peripheral lymphedema. Lymphology 35(2), 46–58 (2002).

35.

Lerner

Klose

Cosimi

: Effective treatment of lymphedema of the extremities. Arch. Surg. 133(4), 452–458 (1998).

36.

Shih

Cormier

: Incidence, treatment costs, and complications of lymphedema after breast cancer among women of working age: a 2-year follow-up study. J. Clin. Oncol. 27(12), 2007–2014 (2009).

37.

Sir Browse

Burnand

Mortimer

: Diseases of the Lymphatics. Oxford University Press Inc., NY, USA 175–176 (2003).

38.

Ridner

Armer

: Post-breast cancer lymphedema: part 2. Am. J. Nurs. 109(8), 34–41 (2009) (Quiz 42).

39.

Ridner

: Symptoms and co-morbidities associated with breast cancer treatment-related lymphedema. Lymph. Link. 17(3), 1–2, 24 (2005).

40.

Rosedale

: Breast cancer survivors' experiences of lymphedema-related symptoms. J. Pain Symptom Manage. 38(6), 849–859 (2009).

41.

Chen

Haber

Guth

Axelrod

: The effect of providing information about lymphedema on the cognitive and symptom outcomes of breast cancer survivors. Ann. Surg. Oncol. DOI: 10.1245/s10434–010–094l–3 (2010) (Epub ahead of print).

42.

Kilbreath

Ward

Lane

: Effect of air travel on lymphedema risk in women with history of breast cancer. Breast Cancer Res. Treat. 120(3), 649–654 (2010).

43.

Abedin

: Benefits seen in postcancer weight-lifting. Time, 12 August (2009).

44.

Ahmed

Thomas

Yee

Schmitz

: Randomized controlled trial of weight training and lymphedema in breast cancer survivors. J. Clin. Oncol. 24(18), 2765–2772 (2006).

45.

De Rezende

Fraco

De Rezende

Morais

Gurgle

: Two exercise schemes in postoperative breast cancer: comparison of effects on shoulder movement and lymphatic disturbance. Tumori 92(10), 55–61 (2006).

46.

Schmitz

Ahmed

Troxel

: Weight lifting in women with breast-cancer-related lymphedema. N. Engl. J. Med. 361(7), 664–673 (2009).

47.

Important paper in the field of lymphedema.

48.

National Lymphedema Network Medical Advisory Committee: Position statement of the national lymphedema network. Topic: treatment www.lymphnet.org/pdfDocs/nlntreatment.pdf

49.

Important reference providing evidence in support of current practice.

50.

National Lymphedema Network website www.lymphnet.org

51.

National Lymphedema Network Medical Advisory Committee: Position statement of the national lymphedema network. Topic: lymphedema risk reduction practices www.lymphnet.org/pdfDocs/nlnriskreduction.pdf

52.

Important reference providing evidence in support of current practice.

53.

National Lymphedema Network Medical Advisory Committee: Position statement of the national lymphedema network. Topic: air travel www.lymphnet.org/pdfDocs/nlnairtravel.pdf

54.

Important reference providing evidence in support of current practice.

Breast Cancer and Lymphedema: A Current Overview for the Healthcare Provider

Abstract

Keywords

Incidence

Diagnosing lymphedema

Treatment

Living with lymphedema

Reducing risk of infection & increased swelling

Air travel

Exercise

Future perspective

Footnotes

References