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13 Combined Clinical and Laboratory (Lymphoscintigraphic) Staging
99
Stage I
• Edema (swelling): mild and/or easily reversible (+)
• Skin change: none without dermatobrosclerosis (DFS) (−)
• Sepsis (systemic and/or local): none (−)
• Daily activity limitation (DAL): no limitation (−)
Stage II
sional limitation (e.g., exercise, hobby) physically,
psychologically and/or socioeconomically
• Edema: moderate and/or reversible with effort (+)
• Skin change: none to minimum without DFS (±)
• Sepsis: none to occasional (±)
• DAL: occasional and/or moderate limitation (±)
• Quality of life (QOL): good with minimal and/or occa-
• QOL: fair with moderate limitation physically, psychologi-
Stage III
cally and/or socioeconomically
to irreversible (±) to (−)
• Edema: moderate to severe and/or minimally reversible
• Skin change: moderate with signicant DFS (+)
• Sepsis: common (+) – less than four times a year
• DAL – frequent and signicant (+)
• QOL – poor with signicant limitation
Stage IV
• Edema: severe and/or irreversible (−)
• Skin change: severe with advanced DFS (╫)
• Sepsis: very frequent (╫) – four times or more a year
• DAL: constant and severe (╫)
• QOL: bad with severe limitation
decreased lymphatic transport (±)
• Dermal backow (DBF): none (−)
• Collateral lymphatics (CL): good visualization (+)
• Main lymphatics (ML): decreased visualization (±)
• Clearance of radioisotope from injection site (CR):
Table 13.2 Guideline criteria for the new clinical and laboratory staging system (I–IV)
Laboratory (lymphoscintigraphic) staging Clinical staging
Grade I (stage) • Lymph node uptake (LN): decreased (±)
• DBF: visualization (+)
* IIA – extent of DBF does not exceed half of each limb
* IIB – exceed half of each limb
• CL: decreased visualization (±)
• ML: poor to no visualization (±)
Grade II (stage) • LN: decreased to none (−)
• CR: more decreased (±)
Grade III (stage) • LN: no uptake (−)
• DBF: visualization (+)
• CL: poor visualization (−)
• ML: no visualization (−)
• CR: no clearance (−)
Grade IV (stage) • LN: none (−)
• DBF: poor to no visualization (−)
• CL: no visualization (−)
• ML: no visualization (−)
• CR: no clearance (−)
*Minimum two or more lymphoscintigraphic findings for laboratory staging and three or more clinical findings for clinical staging
100 B.-B. Lee et al.
Clinical stage is determined based on a total score of various clinical factors
involved: edema (swelling), skin change, sepsis, daily activity limitation, and QoL
(Table 13.2).
The subjective and objective findings of the local condition of the skin and subcutaneous soft tissue are assessed with the degree of skin change (dermatofibroscle-
8,22
rosis),
swelling, and natural reversibility.
The presence of local and/or systemic sepsis is assessed along with the presence
of erysipelas and cellulitis. Functional limitation of daily activity as a result of the
various subjective symptoms is assessed, including pain, uncomfortable sensory
complaints (heaviness, tightness, numbness) and skin texture, feeling of the swollen
limb, and difficulty wearing clothes because of the swelling (Table 13.2).
The evaluation of daily activity limitation was originally included in the QoL
assessment with sepsis; however, this arrangement made interpretation of the clinical status more complicated. Therefore, both items were removed from the QoL
assessment. Only a limited part of the physical condition was left for the QoL
assessment, which incorporates the physical factors, including strength, movement,
restriction of duties at home and work, and psychological and socioeconomical fac-
1,2,20,21
tors
(Table 13.2).
The QoL was evaluated by the impact of the lymphedema on the patient’s physical, psychological, and socioeconomic limitations and well-being (Table 13.1). The
physical factors for the QoL include strength of the affected limb, restriction of
movement compared with the unaffected limb, as well as further additional impact
on duties at home, work, and recreational activity. The psychological factors
included feelings of depression, frustration, anger due to the lymphedema, and difficulty sleeping. The socioeconomic factors included difficulty with intimate relationships and social activities.
1,2
This new clinical staging system could not separate and exclude the economic
factors in the review of the QoL. We learned that patient economic issues have both
social and psychological implications for overall patient well-being.
A separate laboratory staging system using four grades (stages) was developed
based on lymphoscintigraphic findings of the lymphedema.
23-25
Laboratory stage was determined by the sum total of various normal and abnormal findings on lymphoscintigraphy. These findings include the lymph node (LN)
uptake status, the dermal backflow (DB) status, the collateral and main lymphatic
visualization status, and the clearance of the radioisotope (CR) from the injection
site as a parameter of the lymphatic transport ability
1,2
(Table 13.2).
Laboratory staging also has its limitations, although separate staging has sig-
nicantly minimized the confusion associated with staging systems utilizing both
clinical and laboratory data. Clinical staging combined with laboratory staging of
chronic lymphedema is now useful in the treatment decision-making process,
especially with regard to patients with advanced, chronic lymphedema requiring
the timely addition of various reconstructive and ablative surgery where CDT has
26-29
failed.
Several revisions of the new staging systems have been made by a multidisciplinary team through the years, in order to make them more user-friendly.
13 Combined Clinical and Laboratory (Lymphoscintigraphic) Staging
Table 13.3 Demographic data of the initial clinical and laboratory stage of chronic lymphedema
Clinical (C) stage
I 77 53 19 1 0 4
II 98 6 66 24 1 1
III 29 0 2 15 10 2
IV 16 0 1 6 9 0
Total 220 59 88 46 20 7 (total)
220 patients, selected for a 4-year follow-up assessment (1995–2004)
a
Based on the new four-stage system
b
Unavailable for the comparison study
Table 13.4 Demographic data of the clinical (C) stage of chronic lymphedema in progress
(deterioration or improvement)
Initial C-stage Final (progress) C-stage
Clinical stage Clinical stage
I 77 70 6 1 0 0
II 98 3 81 11 2 1
III 29 2 14 12 1
IV 16 1 6 9
Four year follow-up evaluation of the complex decongestive physiotherapy (CDP)-based therapy
results among 220 patients
a
Laboratory (L) stage (grade I–IV)
I II III IV Unidentified
I II III IV Further deterioration
101
b
Clinical Experience
1,2
Among a total of 840 chronic lymphedema patients, 220 patients (85 primary and
135 secondary: 169 female and 51 male: mean age 41.3 years ) were randomly
selected during the period 1995 through 2004 to be evaluated using new clinical and
laboratory staging systems (Table 13.2).
The patients underwent various combinations of standard CDT and compression
therapy. Periodic clinical evaluation was made with an average interval of 6 months,
but no longer than a year’s interval. Lymphoscintigraphic study was performed on a
annual basis, except in situations where recurrent sepsis was present. In these cases,
an additional study was performed whenever feasible.
A comparison of clinical (C) stage and laboratory (L) stage during the initial
diagnosis of 220 patients showed a broad overlap between the two different stagings; each group of patients with the same C stage, had various L stages, and patients
with the same L stage also had a wide range of C stages. In general, a more advanced
L-stage patient was more likely to have a more advanced C stage (Table 13.3).
Clinical implementation of this new staging system (Table 13.4) demonstrated
reliable staging regarding both the progression of lymphedema and improvement of
the clinical status following therapy.
102 B.-B. Lee et al.
Among 220 patients, 49 patients were appropriately classified by this new stag-
ing: 43 had deterioration and 6 showed improvement in their clinical stage.
Deterioration of the clinical stage occurred despite adequate therapy in various C
stages, but was more frequent among patients with advanced C stage, which was
mainly related to decreased compliance.
The majority of patients who deteriorated at the same clinical stage were among
the higher L-stage accompanying group: 5 out of the 7 in C-stage I who progressed
had L-stage II (4/5) and III (2/5) initially, while 10 out of the 14 in C-stage II who
progressed also had a higher L-stage III (9/10) and IV (1/10) from the beginning.
Another 11 out of the 13 in C-stage III, who progressed, had L-stage IV or higher
before treatment.
Maintenance of the initial clinical stage throughout the 4 year follow-up period
was achieved in the majority of patients (171/220) with good to excellent compliance. Further improvement in the C stage was observed in a limited number of
patients, particularly among the excellent compliance group with a good motivation, reversing the C stage (Table 13.4). Two out of the 3, converted from C-stage II
to I, and showed a concomitant improvement in the L-stage from II to I.
This limited experience with a new, combined, clinical and laboratory staging
system appears to be useful in guiding surgical therapy. Using the staging system
allowed earlier determination of treatment failure in patients with minimal
clinical improvement with CDT and allowed optimal timing of various surgical
therapies during the appropriate stage of chronic lymphedema as a supplement to
failed CDT.
Patients experiencing progression of lymphedema by C stage, despite maximum
CDT, benefited from reconstructive surgery
7,11,29
when surgery was added during an
earlier C stage, before a minimum of 2 years in order to become a surgical candidate
when C-stage patients were also classified as having advanced L stage. The excisional surgery
26-29
was also added to the lymphedema in C-stage III and IV, based on
the same principle.
The addition of laboratory staging in the development of this new clinical staging
system has improved the overall predictability of treatment outcome with regard to
clinical response to various therapies and progression of the lymphedema. A patient
with an advanced L-stage, compared with lymphedema patients in the same C stage,
demonstrated a tendency to progress faster in this study.
Therefore, L-stage has been used to help determine which lymphedema patients
would benefit from different treatment modalities, particularly surgical therapy in
order to prevent further disease deterioration.
Conclusion
The two separate staging systems described may be useful in establishing guidelines for the treatment of chronic lymphedema and in the decision-making process
13 Combined Clinical and Laboratory (Lymphoscintigraphic) Staging
103
for supplemental surgical therapy. Further clinical implementation of the staging
systems is still needed to prove its clinical efficacy, especially in defining the role of
surgical therapy.
References
1. Lee BB, Bergan JJ. New clinical and laboratory staging systems to improve management of
chronic lymphedema. Lymphology. 2005;38(3):122-129.
2. Lee BB. Classication and staging of lymphedema. In: Tredbar LL, Morgan CL, Lee BB,
Simonian SJ, Blondeau B, eds. Lymphedema-Diagnosis and Treatment. London: Springer;
2008:21-30:chap 3.
3. International Society of Lymphology. The diagnosis and treatment of peripheral lymphedema.
2009 consensus document of the International Society of Lymphology. Lymphology. 2009;
42:51-60.
4. International Society of Lymphology Executive Committee. The diagnosis and treatment of
peripheral lymphedema. Lymphology. 1995;28:113-117.
5. Lee BB, Villavicencio JL. Primary lymphedema and lymphatic malformation: are they the two
sides of the same coin? Eur J Vasc Endovasc Surg. 2010;39:646-653.
6. Lee BB. Chronic lymphedema, no more stepchild to modern medicine! Eur J Lymphology.
2004;14(42):6-12.
7. Lee BB, Kim DI, Whang JH, Lee KW. Contemporary management of chronic lymphedema –
personal experiences. Lymphology. 2002;35(Suppl):450-455.
8. Olszewski WL. Episodic dermatolymphangioadenitis (DLA) in patients with lymphedema of
the lower extremities before and after administration of benzathine penicillin: a preliminary
study. Lymphology. 1996;29:126-131.
9. Hwang JH, Lee KW, Chang DY, et al. Complex physical therapy for lymphedema. J Korean
Acad Rehabil Med. 1998;22(1):224-229.
10. Szolnoky G, Lakatos B, Keskeny T, Dobozy A. Advantage of combined decongestive lym-
phatic therapy over manual lymph drainage: a pilot study. Lymphology. 2002;35(Suppl):
277-282.
11. Lee BB. Current issue in management of chronic lymphedema: personal reection on an expe-
rience with 1065 patients. Commentary. Lymphology. 2005;38:28.
12. Case TC, Witte CL, Witte MH, et al. Magnetic resonance imaging in human lymphedema:
comparison with lymphangioscintigraphy. Magn Reson Imaging. 1992;10:549-558.
13. Yeo UC, Lee ES, Lee BB. Ultrasonographic evaluation of the lymphedema. Ann Dermatol.
1997;9(2):126-131.
14. Ketterings C, Zeddeman S. Use of the C-scan in evaluation of peripheral lymphedema.
Lymphology. 1997;30:49-62.
15. Szuba A, Shin WS, Strauss HW, Rockson S. The third circulation: radionuclide lymphoscin-
tigraphy in the evaluation of lymphedema. J Nucl Med. 2003;44(1):43-57.
16. Azevedo WF, Boccardo F, Zilli A, et al. A reliable and valid quality of life in patients with
lymphedema – version of the SF-36. Lymphology. 2002;35(suppl):177-180.
17. Launois R, Mègnigbêto AC, Pocquet K, Alliot F. A specic quality of life scale in upper limb
lymphedema: the ULL-27 questionnaire. Lymphology. 2002;35(suppl):181-187.
18. Nieto S. Stages of lymphedema according to correlation among pathophysiology, clinical fea-
tures, imaging and morphology of the affected limbs. Lymphology. 2002;35(suppl):163-167.
19. Bruna J, Miller AJ, Beninson J. The clinical grading and simple classification of lymphedema.
Lymphology. 2002;35(suppl):160-162.
20. de Godoy JMP, Braile DM, de Godoy MF, et al. Quality of life and peripheral lymphedema.
Lymphology. 2002;35:72.
104 B.-B. Lee et al.
21. Johansson K, Ohlsson K, Ingvar C, et al. Factors associate with the development of arm
lymphedema following breast cancer treatment: a match pair case-control study. Lymphology.
2002;35:59.
22. Foldi E. Prevention of dermatolymphangioadenitis by combined physiotherapy of the swollen
arm after treatment for breast cancer. Lymphology. 1996;29:48-49.
23. Hwang JH, Lee KW, Lee BB. Improvement of lymphatic function after complex physical
therapy. J Korean Acad Rehabil Med. 1998;22(3):698-704.
24. Choi JY, Hwang JH, Park JM, et al. Risk assessment of dermatolymphangioadenitis by lym-
phoscintigraphy in patients with lower extremity lymphedema. Korean J Nucl Med.
1999;33(2):143-151.
25. Hwang JH, Kwon JY, Lee KW, et al. Changes in lymphatic function after complex physical
therapy for lymphedema. Lymphology. 1999;32:15-21.
26. Kim DI, Huh S, Lee SJ, Hwang JH, Kim YI, Lee BB. Excision of subcutaneous tissue and
deep muscle fascia for advanced lymphedema. Lymphology. 1998;31:190-194.
27. Huh SH, Kim DI, Hwang JH, Lee BB. Excisional surgery in chronic advanced lymphedema.
Surg Today. 2003;34:434-435.
28. Lee BB. Surgical management of lymphedema. In: Tredbar LL, Morgan CL, Lee BB, Simonian
SJ, Blondeau B, eds. Lymphedema: Diagnosis and Treatment. London: Springer; 2008:55-
63:chap 6.
29. Lee BB, Kim YW, Kim DI, Hwang JH, Laredo J, Neville R. Supplemental surgical treatment
to end stage (stage IV–V) of chronic lymphedema. Int Angiol. 2008;27(5):389-395.
Chapter 14
Early Diagnosis in Latent Phase
Leigh C. Ward
Lymphedema is typically characterized by the time of onset (staging) and the
severity of the symptoms (grading). Various staging schemes have been proposed,
but increasingly most use a four-stage scale: stage 0, a latent or subclinical phase
when swelling is not evident, although lymphatic insufficiency is presumed; stage I,
accumulation of tissue fluid that generally resolves with elevation of the affected
limb with minimal swelling (<20% increase); stage II, when elevation fails to reduce
a moderate amount of swelling (20–40% increase) and pitting edema is present; and
stage III, irreversible, severe (>40% increase) swelling is present and the tissue is
fibrotic.1 Despite the absence of outward clinical signs of lymphedema in the latent
stage, lymphoscintigraphy or lymphangiography shows disrupted lymphatic function.2 Detection of patients in the latent phase has been recognized as important for
identification of those in whom advanced lymphedema may occur.3 This enables
therapeutic intervention at the earliest opportunity, which has been shown to be
more effective than intervention after lymphedema has become established,4 but this
approach is predicated on the ability to detect lymphedema in the latent phase.
A wide variety of objective methods, other than clinical examination, are available for the detection of lymphedema.5 However, many are either technologically
complex (e.g., magnetic resonance imaging [MRI] or dual energy X-ray absorptiometry [DEXA]), invasive, and involve a radiation hazard (e.g., isotopic lymphoscintigraphy) or are otherwise not suitable for routine clinical use because of cost,
e.g., computed tomography (CT). The most commonly used techniques for lymphedema detection are those based on detecting an increase in volume due to the
presence of edema and include water displacement, opto-electrical perometery, bioelectrical impedance and circumferential measurements. Unfortunately, because, by
definition, the latent phase of lymphedema is that prior to detectable swelling, the
utility of such techniques is questionable. Nevertheless, such methods are currently
L.C. Ward
School of Chemistry and Molecular Biosciences,
The University of Queensland, Queensland, Australia
B.-B. Lee et al. (eds.), Lymphedema,
DOI 10.1007/978-0-85729-567-5_14, © Springer-Verlag London Limited 2011
105
106 L.C. Ward
Table 14.1 Accuracy and precision of methods for assessment of lymphedema of the limbs
Method Accuracy Precision and reproducibility
Impedance <±1% ICC > 0.94 (15 W, ~4%)
Water displacement ±0.5% ICC > 0.94 (81 mL, ~4%)
Perometry ±2% ICC > 0.99 (81 mL, ~ 4%)
Tape measurement ±1% ICC > 0.95 (85 mL, ~4%)
ICC intra-class correlation coefficient
a
Absolute values and approximate percentage of measured value
a
References
8,9
10-13
8,10,13
8,12,13
accepted as the best measurement options to detect pre-clinical lymphedema.6 Stout
Gergich and colleagues4 defined a 3% change in volume from a baseline or preoperative measurement in the case of secondary lymphedema as a diagnostic criterion for subclinical lymphedema. They further suggested that, in the absence of
perometry, (which was used in their study), other tools that assess swelling, such as
water displacement, bioimpedance or girth measurements, may be equally useful.
Unfortunately, there are no universally recognized diagnostic criteria for each
of these methods and equivalence between instruments has not been defined.
Furthermore, assessment of lymphedema lags behind many other branches of science where standardization of measurement has long been recognized as the key to
quality control and assurance. Preference should be given to methods of assessment
that meet accepted standards for accuracy, precision, sensitivity, and specificity of
measurement, and that are practical and applicable for routine clinical use.
7
Accuracy can be difficult to assess because the “true” value, i.e., the smallest
change in the measured parameter (volume, impedance, or girth) presumptive of
lymphedema, is unknown. It is necessary to resort to using “phantoms” of precisely
known characteristics, such as cylinders of known volume or electronic circuits of
known impedance. Precision or reproducibility of measurement is more easily
determined from repeated measurements, using either phantoms or human subjects.
Published data, summarized in Table 14.1, suggests that the various methods used
to assess early-stage lymphedema perform similarly with an accuracy of about ±1%
and reproducibility of approximately ±4% standard error of measurement.
Of greater importance for the detection of sub-clinical lymphedema than absolute accuracy or precision is the limit of detection; the magnitude of difference for a
given measurement parameter that can be reliably detected. This is calculated as the
minimal detectable change (MDC) and is given by 1.96 ±2 SEM (standard error of
measurement).
The MDC for volume measurements is approximately 140 mL, assuming a typical SEM of 50 mL for volumetric measurement. This can be compared with the
generally accepted inter-limb difference of 200 mL used as a detection threshold for
breast cancer-related lymphedema (BCRL). Czernieic et al.8 have shown that a minimum of a 120-mL change is required to account for normal fluctuation in limb
volume in the absence of lymphedema to be confident of an effect while Stout
Gergich and colleagues
4
have recommended a 3% change in perometrically measured volume from a pre-lymphedema baseline measurement as a threshold for
lymphedema treatment intervention. With respect to impedance measurements,
similar calculations suggest a detection limit of approximately 40 W or an inter-limb
14 Early Diagnosis in Latent Phase
Table 14.2 Comparison of potential technologies for the early detection of lymphedema
Cost Portability Ease of use
Impedance Low to high High High Low High Low
Perometry Very high None to
medium
Tape Very low High High High Medium
Water displacement Very low Low Medium
High Low High Low
to high
Time
involved
Medium Low Low
Patient
convenience
to high
107
Operator
skills
Low
ratio difference of 0.04 in BCRL.8 Again, larger change is required (a ratio of 0.08)
to account for normal fluctuation of approximately 4.8%.8 We should, however,
question the relevance of this to the detection of pre-clinical lymphedema. By definition, lymphedema in the latent phase is prior to a detectable change in volume. On
this basis, simple volumetric measurements, irrespective of how small the limit of
detection, can never be used for lymphedema assessment at this early stage. Equally,
bioimpedance techniques are not suitable either, since the magnitude of changes in
impedance equate to changes of comparable magnitude in volume.
A more pragmatic approach is to assess promising technologies on the basis of
their practicality in use and sensitivity and specificity for detection at the earliest
opportunity. Surprisingly, relatively few studies have been undertaken. Despite detection thresholds such as a 200-mL volume difference being widely promulgated, the
evidence base for their validity is sparse and sensitivity and specificity analyses are
few in number.7 Box et al.14 demonstrated a 100% confirmation of BCRL in women
when using a 200 mL detection threshold, but this cannot be classed as latent phase
lymphedema. Hayes et al.15 showed, again in women with BCRL, that compared
with bioimpedance, set at 100%, circumferential measurements of the arm had good
specificity (88–100%), but much worse sensitivity (35%). The data of Cornish et al.16
are perhaps most persuasive that bioimpedance, at least, may be capable of detecting
changes indicative of impending lymphedema at an early stage. In a prospective
study, BCRL was detectable by bioimpedance up to 10 months prior to clinical confirmation. This study has yet to be confirmed and extended to other forms of lymphedema, but provides encouragement that using relatively simple non-invasive
technology lymphedema may be detectable in the latent phase or at least prior to
observable changes in volume. The sensitivity of impedance assessment over other
diagnostic modalities is supported by the theory on which the technology is based.
The impedance that is measured is solely that of the extracellular fluid, which includes
the lymph.17 In contrast, simple volume measurement, be it by water displacement,
perometry or tape measure, is that of the total tissue and may be confounded by
changes in tissue compartments other than lymph, e.g., adipose tissue mass.
Detection of latent phase lymphedema implies screening of at-risk individuals. It
is therefore important that the instruments adopted for assessment are fit for this
purpose. Ease of use and cost are important considerations in the uptake of technologies into routine clinical practice. All of the methods referred to above have
their advantages and disadvantages (Table 14.2). A tape measure is inexpensive to
108 L.C. Ward
purchase and is, undoubtedly, easy to use, but its use is time-consuming. Perometry
is also easy to use and rapid to perform, but initial equipment costs are high. Water
displacement is inexpensive, but may not always be suitable, for example, where
there are infections or wounds. Impedance is rapid to perform, with modest cost
(dependent upon instrumentation), but its utility for all forms of lymphedema has
yet to be established.
In conclusion, detection of lymphedema in the latent phase poses significant
challenges. The definition of latent phase or sub-clinical lymphedema that it is prior
to appearance of swelling appears to preclude many of the methods currently used
to detect lymphedema. Other than technologies that measure lymphatic function,
such as lymphoscintigraphy, covered elsewhere in this volume, tools in current use
without exception measure volume either directly or indirectly as in the case of
impedance. Nonetheless, the routine use of these techniques is of clinical value,
particularly where change compared with baseline measures are available, as shown
by the work of Stout Gergich.4 Maximum benefit will be gained by routine surveillance of those at risk of developing lymphedema. At present, the tool most suited for
this purpose appears to be impedance in that it is suitable for home use by those at
risk of or with incipient lymphedema.18 It would be remiss, however, not to additionally acknowledge the importance of self-report by those with lymphedema.
Objective assessments in current use may simply not be measuring the correct
parameters that characterize the subtle early changes in tissue morphology and
physiology that occur in the latent phase. These may, however, be apparent to the
patient. Much additional research into the biology of the development of early-stage
lymphedema is required to allow us to determine the optimal detection strategy.
References
1. International Society of Lymphology. The diagnosis and treatment of peripheral lymphedema.
Consensus document of the International Society of Lymphology. Lymphology. 2003;36:84-91.
2. Bagheri S, Ohlin K, Olsson G, Broroson H. Tissue tonometry before and after liposuction of
arm lymphedema following breast cancer. Lymphat Res Biol. 2005;3:66-80.
3. Campisi C, Boccardo F. Lymphedema and microsurgery. Microsurgery. 2002;22:74-80.
4. Stout Gergich NL, Pfalzer LA, McGarvey C, Springer B, Gerber LH, et al. Preoperative assess-
ment enables the early detection and successful treatment of lymphedema. Cancer. 2008;
112:2809-2819.
5. Rockson SG. Lymphedema. Am J Med. 2001;110:288-295.
6. Piller N, Keeley V, Ryan T, Hayes S, Ridner S. Early detection: a strategy to reduce risk and
severity? J Lymphoedema. 2009;4(1):89-95.
7. Ward LC. Is BIS ready for prime time as the gold standard measure? J Lymphoedema.
2009;4(2):52-56.
8. Czerniec SA, Ward LC, Refshauge KM, et al. Assessment of breast cancer related arm lym-
phedema – comparison of physical measurement methods and self-report. Cancer Invest.
2010;28:54-62.
9. Oldham NM. Overview of bioelectrical impedance analyzers. Am J Clin Nutr. 1996;64:
405S-412S.
10. Man IOW, Markland KL, Morrissey MC. The validity and reliability of the Perometer in evalu-
ating human knee volume. Clin Physiol Funct Imaging. 2004;24:352-358.