Abstract
Background Lymphedema is a common complication of cancer treatment, resulting in swelling and subjective symptoms. Reliable and valid measurement of this side effect of medical treatment is important.
Purpose The purpose of this study was to provide best evidence regarding which measurement instruments are most appropriate in measuring lymphedema in its different stages.
Data Sources The PubMed and Web of Science databases were used, and the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines were followed.
Study Selection Clinical studies on measurement instruments assessing lymphedema were reviewed using the Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2) scoring instrument for quality assessment.
Data Extraction Data on reliability, concurrent validity, convergent validity, sensitivity, specificity, applicability, and costs were extracted.
Data Synthesis Pooled data showed good intrarater intraclass correlation coefficients (ICCs) (.89) for bioimpedance spectroscopy (BIS) in the lower extremities and high intrarater and interrater ICCs for water volumetry, tape measurement, and perometry (.98–.99) in the upper extremities. In the upper extremities, the standard error of measurement was 3.6% (σ=0.7%) for water volumetry, 5.6% (σ=2.1%) for perometry, and 6.6% (σ=2.6%) for tape measurement. Sensitivity of tape measurement in the upper extremities, using different cutoff points, varied from 0.73 to 0.90, and specificity values varied from 0.72 to 0.78.
Limitations No uniform definition of lymphedema was available, and a gold standard as a reference test was lacking. Items concerning risk of bias were study design, patient selection, description of lymphedema, blinding of test outcomes, and number of included participants.
Conclusions Measurement instruments with evidence for good reliability and validity were BIS, water volumetry, tape measurement, and perometry, where BIS can detect alterations in extracellular fluid in stage 1 lymphedema and the other measurement instruments can detect alterations in volume starting from stage 2. In research, water volumetry is indicated as a reference test for measuring lymphedema in the upper extremities.
Lymphedema is a complex problem that can occur in any body part. Primary lymphedema develops as a result of dysfunction or malformation of the lymphatic system. It is assumed to occur in 1.15/100,000 people aged over 20 years.1 Patients with lymphedema experience swelling and impairments, limitations, and restrictions in functioning and encounter environmental factors, as described in the International Classification of Functioning, Disability and Health (ICF) core set for lymphedema.2 Secondary lymphedema is caused by disruption of the lymphatic system, mostly as a result of cancer treatment and especially after lymph node dissection or radiotherapy to the lymph nodes and in patients with advanced cancer.3 The incidence differs per tumor type, area, and stage, from 5% after sentinel node biopsy in breast cancer to 42% in cervical cancer.4
In patients suspected with lymphedema, a thorough examination on the origin of the swelling is required to exclude other reasons of swelling. Stages of lymphedema have been described by the International Society of Lymphedema, ranging from subclinical edema (stage 0) to hard (fibrotic) edema (stage 3).5 In stage 0, no volume change is observed. In stage 1 volume change is transient. Generally, patients complain about subjective symptoms such as a feeling of heaviness, numbness, or tingling.6 To get insights into these symptoms, lymphedema-specific questionnaires or symptom lists can be used.3 In stage 1 of lymphedema, the amount of extracellular water or subcutaneous water can be measured to quantify lymphedema. The ratio between the amount of total body water and extracellular fluid can be measured by bioimpedance spectroscopy (BIS).7 Bioimpedance is a measure of the resistance to the flow of an electric current through the body or a body part. It is a noninvasive method of measuring body composition, and usually frequencies from 4 kHz to 1 MHz are used. The MoistureMeter (Delfin Ltd, Kuopio, Finland) measures the percentage of water under the skin (tissue dielectric constant) using a probe with a 300-MHz signal.8 Swelling occurs from stage 2 lymphedema. Swelling of limbs can be measured by water displacement (volumetry or inversed volumetry), perometry, or circumferential tape measurements.9 A special device for circumferential measurements is a perimeter, a bar with tape at every 4 cm and with a 20-g weight at the end of each tape.10 In later stages, accumulation of adipose tissue and fibrotic alterations change the consistency of the lymphedema, and especially stage 3, the resistance in the skin and subcutaneous tissue can be measured by tonometry.11
Prevention and early detection of lymphedema are important because early treatment results in less burden for the patient and is cost-effective.12 The most common treatment for lymphedema consists of manual lymphatic drainage, compression therapy, exercises, and skin care.5
To our knowledge, no systematic literature review has been published assessing the measurement properties of clinical instruments for measurement of lymphedema. A complicating factor is that a clear gold standard for lymphedema measurement is lacking. In research and in clinical settings, different measurement instruments are used, without consensus on the best measuring method. Moreover, in the midline (head and neck, breast, trunk, or genitalia), lymphedema volume or circumference measurements are difficult to perform. In this systematic review, we focus on instruments for measuring and monitoring lymphedema. Ideally, the measurement instrument must be easily applicable, short in measurement time, inexpensive, and acceptable by the clinician and the patient.
The primary question in this review was: Which instruments are most appropriate in measuring and monitoring lymphedema? Specific questions to be answered were: (1) Which measurement instruments are described in peer-reviewed literature, and which edema aspect is measured? (2) Which measurement instrument is most reliable and can be indicated as most appropriate for measuring lymphedema based on test-retest reliability, lowest standard error of measurement (SEM), and smallest detectable change (SDC)? and (3) Which measurement instruments are reliable and feasible for application in clinical practice, considering different stages of lymphedema and different locations of the body?
Method
Data Sources and Searches
We conducted a systematic literature search conforming to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines for identifying instruments for measuring lymphedema using the databases of PubMed and Web of Science until November 11, 2015. Published studies in English, Dutch, French, and German languages were eligible for inclusion. No limit on date of publication was applied. The search string was developed according to recommendations for sensitive search of measurement properties of the COnsensus-based Standards for the selection of health Measurement INstruments (COSMIN) group.13 See eAppendix 1 for the full search string.
Target Population
Studies in patients with lymphedema or at risk for developing lymphedema, regardless of whether compared with healthy controls, were included.
Inclusion Criteria
Prognostic, cross-sectional, and case-control studies assessing measurement properties of clinical measurement instruments for lymphedema with at least 2 repeated measurements with one instrument and studies describing comparisons between 2 or more measurement instruments were included.
Exclusion Criteria
Intervention studies not evaluating properties of measurement instruments related to lymphedema and studies in a healthy population were excluded. Measurement instruments such as computed tomography, magnetic resonance imaging, dual-energy x-ray absorptiometry scan, caliper, goniometer, and weighing scale/body mass index were excluded. We also excluded studies where healthy controls were involved with a difference in mean age of more than 10 years between study groups. Studies that used only patient-reported questionnaires, retrospective studies, and conference papers also were excluded.
Study Selection
Initial study selection was performed by the first author (J.T.H.). Two independent authors (J.T.H. and P.B.V.) reviewed the list of articles based on title and abstract. Full-text articles were then retrieved and examined independently to obtain a final list of eligible studies. If consensus could not be achieved, the review team adjudicated.
Quality Assessment
We defined lymphedema as a difference between left and right extremities or between measurements in case of 2-sided or midline involvement. The Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2) scoring instrument was used to evaluate the quality of the initially selected studies.14 The QUADAS-2 scoring instrument includes 4 domains in assessing the quality of the studies: patient selection, index instrument, comparator instrument, time and flow. Two researchers (J.T.H. and P.B.V.) independently scored each item of the QUADAS-2 scoring list. Disagreements were discussed together to reach consensus. Items with low risk of bias or no concern regarding applicability were assigned a quality score of “+,” those with unclear risk of bias or concern regarding applicability were assigned a quality score of “?,” and those with high risk of bias or serious concerns regarding applicability were assigned a quality score of “−.” The decision criteria are described in Table 1. The total test score per domain was estimated as the median of all “risk of bias” criteria within that domain. For each domain, an overall score of more than “?” indicated low risk of bias or no major concerns and was marked as “+,” an overall score of “?” indicated medium risk of bias and was marked as “?,” and an overall score of less than “?” indicated high risk of bias and was marked as “−.” Eligible studies for inclusion in data synthesis needed to have an overall low risk of bias in the domain “method of patient selection” and overall medium or low risk of bias in the domains “index test” or “comparator test.” As advised by Whiting et al,14 a total score was not generated, and conclusions were based on domain scores.
Items of Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2): Risk of Bias and Applicability Concerns Specified for Lymphedema Measurementsa
Data Extraction
The following measurement properties of identified instruments in the included studies were extracted by one reviewer (J.T.H.) and verified by a second reviewer (C.B.): intraclass correlation coefficients (ICCs) for estimating measurement differences within raters (ICCintra) and between raters (ICCinter); SEM for estimating the measurement error; SDC for estimating which change in measurement outcome will be clinically relevant; concurrent validity and convergent validity to estimate whether the instruments measure the same construct; and sensitivity and specificity to estimate the difference in interpretation concerning the presence of lymphedema between the comparator test and other measurement instruments. Concurrent validity was defined as comparison of outcomes between tests or between groups, administered at the same time, based on their correlation. Convergent validity was assessed by comparing similarity of different procedures of a certain measurement instrument, based on their correlation. If available, results regarding applicability and costs were extracted as well.
Data Synthesis and Analysis
For quantitative analysis on reliability, the following measurement properties for each measurement instrument were extracted: ICC, SEM, SDC, sensitivity, and specificity. Where ICCs were reported for each level of tape measurement, mean ICC and standard deviation were calculated. Where possible, data were pooled to estimate ICC. For statistical pooling of data, the Fisher estimated r to z transformation for ICC was used, in which the number of examiners and participants are included in the formula. The SDC was calculated from the standard deviation of the difference (SDdifference) or, when not available, derived from the SEM. The weighted mean SEM and SDdifference were calculated based on the number of included participants in the studies. Variance (σ) of SEM and SDC was calculated based on the pooled data in relation to the data in the original studies. When data of different calculations for tape measurement were available, data from the frustum method were extracted (for formulas, see eAppendix 2). When different distances between tape measurements were used, the measurement nearest to 4 cm was used. Based on the highest ICC with the lowest SEM, SDC, and variance, the most appropriate measurement instrument for measuring lymphedema was indicated as the reference test. Concurrent validity, sensitivity, and specificity were described in relation to the comparator test. Correlations among measurement instruments or measurement procedures were interpreted as follows: r>.75 is excellent and r=.40 to .75 is fair to good.15 Intraclass correlation coefficients were interpreted as follows: r>.90 is high and r>.80 is good.
Results
Included Studies
We identified 631 unique studies, of which 103 were eligible for full-text assessment. Two references used in these studies were included as well (Figure). Of these studies, 51 studies were excluded because they did not meet the inclusion criteria. Exclusion of these studies resulted in the initial selection of 54 articles representing 50 unique studies. Four studies were reported in more than one article, which were assessed together. Forty-one studies compared 2 or more measurement instruments. In general, testers were not blinded to the patient's condition and outcome of the index or comparator test. In most studies, tests were conducted directly after each other. Therefore, we cannot rule out that the test procedures did not result in bias (Tab. 2).
Flow diagram of literature search of measurement instruments for lymphedema. QUADAS-2=Quality Assessment of Diagnostic Accuracy Studies-2.
Quality of the Assessed Studies, Following Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2) and the Criteria Specified in Table 1a
All studies were conducted in hospital settings. Four studies16–19 were not conducted in Western countries. Most studies were conducted in female participants. In 5 studies,11,20–23 both female and male participants were included.
Fifteen studies reported reliability using ICC; SEM was reported in 9 studies, and SDC was reported in 2 studies. Concurrent validity was reported in 16 studies, and convergent validity was reported in 8 studies.
The following measurement instruments were described for measuring and monitoring lymphedema: water volumeter, tape measure, perometer, bioimpedance spectroscope, MoistureMeter, and tonometer. Eight articles7,11,24–29 compared tape measurement with BIS. Seven articles23,28,30–34 compared perometry with BIS. Four studies22,35–37 investigated BIS. Two studies8,38 compared tape measurement with the MoistureMeter. Two studies39,40 solely investigated the MoistureMeter. Twenty-one articles6,9,10,16–18,21,41–54 compared water volumetry with tape measurement. One study55 solely investigated tape measurement. Ten articles6,9,21,28,31,32,50,51,54,60 compared tape measurement with perometry. Four articles57–60 solely investigated perometry. Seven studies6,9,21,50,51,54,61 compared volumetry with perometry. One study62 compared volumetry with tonometry. Four studies11,16,19,63 compared tape measurement with tonometry. One study64 compared tonometry with BIS in the breast.
None of the studies described measurement properties in different stages of lymphedema. Based on the methodological assessment, we finally included 30 articles (27 studies) with sufficient quality for further analysis. Study characteristics of the included studies are described in Table 3 and are further analyzed and summarized in Table 4.
Characteristics of the Studies on Measurement Instruments in Lymphedema Selected After Quality Assessment of Diagnostic Accuracy Studies-2 (QUADAS-2) Evaluationa
Measurement Properties of Included Studiesa
Reliability
Reliability for measuring lymphedema using BIS was described in 3 studies. Intrarater reliability values ranged from .88 to .99.11,32,33 In the upper extremities, the ICC was .95 for the subgroup with lymphedema and .81 for the subgroup without lymphedema.32 Pooled ICC data for the lower extremities showed an ICCintra of .89 (95% confidence interval [CI]=.88, .90).11,33
Reliability for measuring lymphedema using the MoistureMeter was described in one study: the ICCinter was .63 (95% CI=.43, .79) for the foot, .94 (95% CI=.89, .97) for the ankle, and .94 (95% CI=.88, .97) for the lower leg.40
Reliability for measuring lymphedema in the upper extremities using water volumetry was reported in 10 studies.9,10,16,42–44,46,47,49,53 Pooled ICC data of the studies showed ICCintra9,42–44,46,47,49 and ICCinter9,16,42,44,46,47 values of .99 (95% CI=.99, .99). The weighted mean SEM was 0.7% (σ=0.8%), and the weighted mean SDC was 3.6% (σ=2.7%).9,10,16,42–44,46
Reliability for measuring lymphedema using tape measurement was reported in 12 studies, of which 10 studies of the upper extremities reported ICC values.9,10,32,43–47,49,53 Pooled ICC data in studies of the upper extremities showed an ICCintra value of .99 (95% CI=.99, .99)9,10,32,43–47,49 and an ICCinter value of .98 (95% CI=.98, .98).9,10,43,46,47 The weighted mean SEM was 2.8% (σ=3.2%), and the weighted mean SDC was 6.6% (σ=2.6%).9,10,32,43,44,46 The SDC for the lower extremities was reported in one study55 (intrarater difference=264.1 mL, interrater difference=1,014.5 mL) and was not recalculated to percentual change.
Reliability for measuring lymphedema using perometry was reported in 3 studies.9,21,32 Pooled data of studies of the upper extremities showed an ICCintra value of .99 (95% CI=.97, 1.00).9,32 Interrater reliability was .99.9 The weighted mean SEM was 2.1% (σ=2.6%).9,32 The SDC in the lower extremities was 29.4%.21
Pooled results for reliability are summarized in Table 5. The Fisher estimated r to z is shown in the eFigure.
Pooled Data for ICC, SEM, and Weighted Mean SDCa
Based on the highest ICC with smallest variance and smallest SEM and SDC, we used water volumetry as a comparator test in this article. Water volumetry is indicated for use as a reference test in future research for measuring lymphedema in the upper extremities. Information about measurement of lymphedema in the lower extremities is scarce; therefore, no conclusion could be stated.
Concurrent Validity
In the upper extremities, correlations between water volumetry and tape measurement varied from .80 to .99.10,41,43–49 The correlation between water volumetry and BIS was .83.29
Convergent Validity
Convergent validity was reported in 7 studies of patients with lymphedema. The correlation between different widths of tape and tape measurement was .95,48 the correlations among different measurement intervals varied from .79 to .98,41,46,47 and the correlation between plastic tape and paper tape was .98.49 Convergent validity in studies with different patient groups showed a peak bias in 10- to 20-cm segments of 16.6%,31 and variance in volume occurred mainly in 10- to 20-cm segments and in 20- to 30-cm segments (r2=.77–.95).57
Sensitivity and Specificity
Sensitivity and specificity were reported in 6 studies.17,21,25,27,29,40 In agreement with our analysis of reliability, measurement instruments ideally had to be compared with water volumetry. One study17 compared tape measurement with water volumetry in the upper extremities. Using a cutoff point of 10% volume difference, sensitivity was 0.73, and specificity was 0.78. Using a cutoff point of 200 mL and 2-cm difference at any of 7 measurement points, sensitivity was .90, and specificity was .72.
Variability in Measurement Procedures
In using BIS, the position of the electrodes differed across studies. Used methods were: 3 electrodes placed on the wrists and hands and 1 electrode placed on the foot,29,33 electrodes placed on both wrists and ankles,11 and 2 or 3 electrodes placed at 10-cm intervals in the upper extremities.27,31,32 Based on the results, no conclusion about the best measurement method in BIS could be stated.
Water volumetry was carried out with a device containing water, and water overflow was measured with a weighing scale9,10,41,43,47,62 or a cylindrical measure.16,21,44–46,48,49,53 Damstra et al42 described a new device in which water shortness was measured. Studies using a weighing scale reported ICCintra and ICCinter values of .99. In studies using a cylindrical measure, ICCintra values varied between .94 and .99, and ICCinter values varied between .92 and .99.
Tape measurements were carried out and interpreted in different ways. The starting point was the styloid process of the ulnae. Anatomical points were used as measurement points in 4 studies.17,21,43,49 Measurement intervals differed from 3 to 12 cm. Limb volume was calculated with the truncated cone formula,10,29,32,41,43–49 disk formula,9,47,55 rectangle formula,47 or trapezoidal formula47 or with sum of circumferences.21,27 Hand volume was calculated with the trapezoidal formula47 or figure-of-eight method.53 A flexible, nonstretch tape measure was used in all studies; in some cases, a spring-loaded tape measure was used to ensure equal pressure on the surface of the skin in all measurements. Devoogdt et al10 used a bar with tape at 4-cm intervals. The limb volume difference calculation was handled in different ways: distraction of absolute volumes of limbs, summation of circumferences, calculation of percentage difference, or calculation of relative volume change.
Feasibility
The time needed for measurements of the upper extremities, as reported in the studies, was 8 minutes for tape measurement and 5 minutes for water volumetry,42 1 minute for each lower extremity for perometry,23 and 2 minutes for BIS when electrodes and apparatus were connected.23 The MoistureMeter needed 60 seconds per measurement.8
In BIS measurement, patients have to avoid heavy activity for 2 hours before measurement, remove all jewelry, and empty their bladder. The skin must be cleaned with alcohol. Electric devices such as a pacemaker interfere with the measurement, so these participants were excluded from measurements. Only costs of the tonometer were reported, being Australian $500 in 2011.11
Discussion
Our study showed clear evidence for good reliability of BIS in the lower extremities and for high reliability and excellent validity of water volumetry, tape measurement, and perometry in measuring and monitoring lymphedema in the upper extremities. Water volumetry had the lowest variance, SEM, and SDC in measurement of the upper extremities, but differences in ICCs, SEMs, and SDCs among water volumetry, tape measurement, and perometry in the upper extremities were very small. The correlation between water volumetry as a comparator test and BIS and tape measurement as index tests in the upper extremities was excellent. In addition, we found moderate evidence for good reliability of ICCintra values of BIS in the upper extremities and high reliability ICCinter values for the MoistureMeter and good reliability of the tonometer in the lower extremities.
Based on our analysis, BIS, volumetry, tape measurement, and perometry can be recommended in clinical practice. However, the clinician has to keep in mind that measurement instruments are not interchangeable.43,47 In addition to considering reliability and validity, the choice for a measurement instrument depends on feasibility and costs and is related to the stage of lymphedema. In early stages of lymphedema (stage 0 to early stage 2), BIS can detect alterations in the amount of extracellular fluid earlier than swelling can be detected by volumetric measurement instruments. The MoistureMeter measures subcutaneous water, which alters from stage 0 as well. It is unclear whether subcutaneous water can be measured in the later stages of lymphedema when fibrosis and fat deposit are apparent. Starting from stage 2, swelling of limbs can be measured by volumetry. In the later stages of lymphedema, especially stage 3, the resistance of the skin or fibrosis can be measured by tonometry.
The bioimpedance spectroscope, MoistureMeter, and perometer are expensive measurement instruments compared with the water volumeter or tape measure and, therefore, are less feasible in primary care practice. Moreover, in BIS, expensive electrodes are needed for every measurement. Due to lack of space in primary care practice, it is more difficult to create a permanent location for measuring by water volumetry than in clinical settings, and tape measurement is more feasible. To promote self-management, the patient can be instructed to measure himself or herself or have measurements taken by a family member.49,65,66
Only one study17 described sensitivity and specificity using water volumetry as the reference instrument in the upper extremities. Ideally, a measurement instrument should have high sensitivity to detect every patient with lymphedema and high specificity to exclude false-positive results. The study on measurement of upper extremity lymphedema showed high sensitivity (0.90) of 200 mL in water volumetry and differences in circumference of 2 cm at any point in tape measurement.17 However, the absolute volume difference depends highly on body composition,59 and many patients with breast cancer gain weight during cancer treatment.67 Moreover, differences of less than 2 cm over more measurement points may indicate lymphedema. Future research is needed to analyze different methods of calculating tape measurement compared with water volumetry.
The time needed for measurement and the burden of different measurement instruments were reported scarcely in the included studies. The time to prepare the patient and the measurement instrument were not reported, nor was time to clean the measurement instrument. In tape measurement, the time needed for measurement depends highly on the amount of measurement points. Calculated volume showed small variance among different measurement intervals. Therefore, it is acceptable to choose larger measurement intervals (ie, up to 10 cm). As tape measurement has higher variance compared with water volumetry, with perhaps higher variance in daily practice than in research, special attention is needed for an exact measurement protocol.
Measurement properties of the bioimpedance spectroscope, MoistureMeter, water volumeter, tape measure, perometer, and tonometer were mostly described for measuring lymphedema in the upper extremities and warrant future investigation in the lower extremities and at midline. Volumetry cannot be applied at midline (head, neck, trunk, and genital region). Tonometry was investigated in patients with filariasis, with good measurement properties using a rather high cutoff point for sensitivity analysis. In these patients, consistency of the lymphatic tissue was probably harder, as occurs in advanced stage 2 or 3 lymphedema. In midline, the bioimpedance spectroscope, MoistureMeter, and tonometer are possibly useful instruments because they are more practicable in these body regions. In the lower extremities, tape measurement and perometry are feasible as well; water volumetry requires good range of motion of the hip joint of the patient. The reliability and validity of measurement instruments in these body parts warrant further investigation. For reports of measurement burden, qualitative research in patients at risk for lymphedema or with lymphedema is needed.
Strengths and Weaknesses of the Study
To our knowledge, this is the first systematic review on measurement properties of instruments for measuring and monitoring lymphedema. We succeeded in performing a meta-analysis for reliability of tape measurement, water volumetry, and perometry on measurements in the upper extremities and of BIS in the lower extremities. Based on our analysis, recommendation of the use of water volumetry and tape measurement for measuring lymphedema in the upper extremities is strong, as many studies were included in the meta-analysis.
This study had several limitations. As there was no gold standard as a comparator test, we reviewed all measurement instruments independently. Lymphedema is predominantly described in women with breast cancer and less in gynecological cancer. Medical treatment of these patients results in more risk in developing lymphedema than other types of cancer, except melanoma.4 Therefore, lymphedema is more common and probably investigated more in women than in men. On the other hand, primary lymphedema and filariasis (in tropical countries) are present in both sexes. Diagnosis of filariasis is based on analysis of blood or lymphatics, and measurement of lymphedema is secondary. Measurements in patients with primary lymphedema are poorly described.
Based on the quality of the articles, we included only half of the initially selected articles for further analysis. In the rejected studies, a description of the procedure was lacking, especially in patient selection and measurement protocol. Regarding the risk of bias of the included studies, we noted several concerns. First, patient selection was diverse and not always described; consecutive patients were included in some studies, and random selection or enrollment via advertisement was mentioned. Second, only a few authors described the severity of the lymphedema. Third, measurement protocols of the comparator test were poorly described, especially in studies on perometry, BIS, and MoistureMeter. Fourth, blinding of investigators was clearly described in only 3 studies. Finally, only 9 studies included more than 50 patients, and 2 studies analyzed only a part of the study sample. Therefore, we cannot exclude bias in our review.
Some articles stated that early detection of lymphedema is important and, therefore, recommended expensive tools such as computed tomography or magnetic resonance imaging.68 These modalities are not appropriate for surveillance during treatment of lymphedema due to costs, patient burden, and accessibility. One study12 reported that early detection of lymphedema by perometry and early treatment of lymphedema based on perometry measurement are cost-effective and imply less burden for the patient. As perometry is highly comparable to water volumetry and tape measurement, these measures are suitable for surveillance of lymphedema as well. A widely accepted reference point to start treatment for lymphedema in the upper extremities is defined as a volume difference of 5% to 10% between the extremities.69 Clear cutoff points for the lower extremities are not available. Extensive lymphedema treatment generally starts with volume changes over 10%. It is unclear whether earlier identification of lymphedema makes clinical reasoning different, as special recommendations for prevention of lymphedema will be the same as for all patients at risk for lymphedema. Although the SEM is the smallest amount of change that can reliably be measured, the SEM in volumetric measurement instruments is smaller than normal differences between extremities.70 Therefore, we propose using the SDC as clinical relevant referring point to start treatment of lymphedema. Our review showed weighted mean SDC values of 3.6% for water volumetry, 5.6% for perometry, and 6.6% for tape measurement. Treatment before these cutoff points can lead to overtreatment and has to be avoided.
Implications for Daily Practice and Future Research
Measures with evidence for good reliability and validity are BIS, water volumetry, tape measurement, and perometry, where BIS can detect alterations in extracellular fluid in stage 1 lymphedema, and the other measures can detect alterations in volume starting from stage 2. Based on measurement properties and feasibility, we suggest water volumetry and tape measurement as best practice in measuring lymphedema in the upper extremities. Weighted mean SDCs of the different measures are indicated as the starting level of treatment of preclinical lymphedema. Tape measurements have to be calculated to volume. Volume has to be calculated to percentage difference. The styloid process or lateral malleolus is the starting point for tape measurement.
In future research, measurement protocols and results have to be reported clearly and in a uniform way to allow meta-analysis. We recommend water volumetry using a weighing scale as a reference test in the upper extremities for future research. Measurement of midline lymphedema and lymphedema in the lower extremities warrants more research. More attention in research must be paid to sensitivity and specificity of the clinical measurement instruments in lymphedema. Future investigation of the role of tonometry in patients with advanced stages of lymphedema and in case of fibrosis of the tissue also is needed.
Footnotes
All authors provided concept/idea/research design, writing, data analysis, and consultation (including review of manuscript before submission). Ms Hidding and Dr Beurskens provided data collection. Ms Hidding, Professor van Laarhoven, and Professor Nijhuis-van der Sanden provided project management. Professor Nijhuis-van der Sanden provided facilities/equipment.
The study was registered in Prospero: number CRD42014009079.
- Received July 22, 2015.
- Accepted June 15, 2016.
- © 2016 American Physical Therapy Association
References
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