The authors conducted a systematic review of methods and tools to clinically measure lower-extremity limb and genital lymphedema in urogenital cancers in order to identify reliable, valid, and clinically feasible methods to employ in daily practice. The primary literature search took place from August through September 2015 using 6 electronic databases: Google Scholar, PubMed/MEDLINE, CINAHL, Web of Science, Cochrane Review, and PEDro. Primary search terms that were used included the following: lymphedema, lower extremity, limb volume, measurement of limb volume, and genital lymphedema. Additional search terms that described the measurement of lower-extremity limb volume and lymphedema, and genital lymphedema in addition to the names of specific clinical measuring tools, can be found in the Appendix. Secondary searches through bibliographic review of oncology journals and key research articles took place between October and December 2015.
To be included in this review, studies (1) were published in English; (2) clinically measured limb volume by direct or indirect means preferably of the lower-extremity and/or genitals; (3) reported psychometric properties; (4) presented methods considered clinically feasible in a typical physical therapy practice; and (5) included adults (18 years or older). Measures that are not available to the physical therapist, such as lymphoscintography, fluorescence lymphography, or magnetic resonance imaging, were not included. In addition, self-reported measures of measuring lymphedema were not included, as this review is focused specifically on objective clinical measures. Included articles were considered if published from January 1, 1996, to present, unless a study published prior to 1996 was deemed a key article. Research focusing on participants with lower-extremity or genital lymphedema as a result of urogenital cancers took first priority, followed by upper-extremity lymphedema and/or vascular disorders and venous insufficiency. While searching the databases, when other patient populations in which limb volume measurements were investigated, such as lower-extremity amputations, met all other inclusion criteria, these articles were included when no other evidence in the cancer population was available. While it may appear that the research in upper-extremity lymphedema, vascular disorders or venous insufficiency, and residual limbs is not applicable to this review, the methods of volume measurement, whether water displacement or use of a truncated cone, are based on principles of physics and mathematics and do not change on the basis of the item measured. After retrieving all articles, duplicates were removed, and studies were screened on the basis of title and abstract initially, followed by review of full-text.
Data Extraction and Analysis
Teams of 2 reviewers independently performed data extraction using the Cancer EDGE Task Force Rating Form (Supplemental Digital Content 1, http://links.lww.com/REHABONC/A3). Psychometrics included in the Cancer EDGE Task Force Rating Form consisted of reliability, validity, ceiling/floor effects, sensitivity to change, and clinical utility. The following criteria were applied to determine the strength of the psychometric properties: excellent reliability (≥0.90); good reliability (0.76-0.89); moderate reliability (0.50-0.75); and poor reliability (<0.50).15 Concurrent, discriminative, criterion-related, and construct validity values are reported when available, as well as measures assessing responsiveness to change such as minimal detectable change (MDC) and minimal clinically important difference. In the absence of these common statistical calculations, the coefficient of variation was reported. Determining clinical usefulness was based on equipment needed, cost, ease of use, scoring/interpretation, and availability of normative data. Outcome measures that directly or indirectly measured lower-extremity and genital lymphedema were categorized into 1 of 5 tools: (1) water displacement, (2) tape measure, (3) optoelectric volumetry, (4) bioimpedance, and (5) ultrasound. Each reviewer then rated the measure using the original Cancer EDGE Rating Scale. Any discrepancies in ratings were discussed with all 4 reviewers until consensus was reached.
The initial literature search using terms outlined in the Appendix, alone or in combination, yielded 181 658 articles. After screening for titles and abstracts and removing any duplicates, 68 articles were identified for subsequent review. An additional 8 studies were found on secondary search. No articles were found that met eligibility criteria for the measurement of genital lymphedema. After applying inclusion/exclusion criteria (articles were removed that did not have psychometric properties of interest, or were not published in the date range specified, or were not conducted within populations previously identified), a total of 33 articles were reviewed. Some of the studies included psychometric analysis of more than 1 measure of lymphedema such that the number of articles reviewed for each tool is not mutually exclusive. The numbers reviewed by category are water displacement (11), tape measure (15), optoelectric volumetry (7), bioimpedance (12), and ultrasound (3). Figure 1 outlines the flow diagram for the literature search.
The outcome measures, ratings, and strengths and weaknesses are summarized in Table 3, whereas Table 4 presents the psychometric properties of the Highly Recommended and Recommended measures for measurement of lower-extremity lymphedema. Finally, Table 5 summarizes the clinical usefulness of the recommended measures for lower-leg lymphedema.
Water displacement and tape measure circumferential measurement methods scored a 4 and are Highly Recommended by the Urogenital Cancer EDGE Task Force. Both measures have been extensively tested and used to measure limb volume in persons with lower-extremity edema or lymphedema. Two other measures, optoelectric volumetry and bioimpedance, are rated 3, or Recommended, based on limitations in clinical utility. The use of ultrasound was not recommended (rating of 1) as a measure of lower-extremity lymphedema, due to a lack of available psychometric evidence for use and poor clinical utility. Furthermore, no clinical method can be recommended to measure genital lymphedema, as measures reported in the literature are limited to lymphangiography and magnetic resonance lymphography.
Based on the chronic nature of lymphedema, the accurate and reliable assessment of limb volume is crucial to detect lymphedema and to monitor change in limb volume or amount of lymphedema over time. As lymphedema may not be visibly apparent in its earliest stages, ongoing monitoring of the limb at risk is important to detect any change over time. Limb volume as changes as small as 3% has been documented as preclinical lymphedema in a population of women with breast cancer–related lymphedema.10 It is reasonable to extrapolate these findings in lower-extremity lymphedema in the absence of other research support, as well as support the need to continue to monitor the limb at risk. Direct or indirect measures of lymphedema (limb volume or impedance ratios) can be recorded at baseline prior to medical intervention and used in comparison with a contralateral normal limb, if available, or the same limb over time to assess and track the response to treatment. In the long term, measurements allow for monitoring of the success of the self-management skills that the individual employs. Water displacement, circumferential measurement with a tape measure, optoelectric volumetry, and BIA are recommended tools to monitor lower-extremity limb volume. While the research available lacks specific data indicating how responsive each of these measures are, those measures that can accurately detect small levels of change, such as a 3% volume change or a difference in impedance ratios between limbs, are indicated for use to monitor change in this population.
Water displacement is a method for assessing volume used since first described by Archimedes in Ancient Greece. Archimedes principle, a body submersed in a liquid loses weight equal to that of the volume of liquid that it displaces, provides the basis for limb volume measurement in water.16 Water displacement as a method to calculate the volume of a limb is reproducible using a standardized container, standardized temperature of the water and room, standardized immersion of the limb at the same depth and position, and a standardized way to measure the displaced water.17 , 18 Measuring displaced water is most often done by volume, including the use of a transducer-equipped volumeter, although some studies used the weight of the displaced water.17 , 18 In either method, the involved limb is submerged in a container of water, generally a volumeter, in the same position and to the same depth on each measurement occasion. Limb volume is then based on the measurement of the water displaced.
Water displacement is considered the “criterion standard” of volume measurement to which all other methods are compared.19 Most studies reviewed described the use of water displacement measured volumes to the level of the knee and were done in patients with venous insufficiency or peripheral vascular disease.17 , 18 There were no studies found for full-leg water displacement, most likely reflecting the difficulty that would be encountered in creating a container for volumetric measurement of differing length legs and the attendant difficulty in achieving insertion of a full leg into the device. Water displacement was found to have a high day-to-day reliability in repeated measures done over 5 episodes. Test-retest values ranged from r = 0.95 to r = 0.99, and the mean percent change in volume measurements ranged between 0% and 0.37%.16 Overall interrater reliability of this method varies from ρ = 0.95, where ρ is the intrasubject correlation coefficient, based on an analysis of variance,20 to intraclass correlation coefficient (ICC) = 0.99.21 One study examined the minimum percent change of the volume of the leg and determined the MDC to be 22.2% to 23.4%.22 These excellent psychometric properties make water displacement a Highly Recommended measure of lower-extremity limb volume.
The advantages of water displacement as a method for volume assessment are low cost (generally <$400), with high accuracy in assessing the most distal portion of the limb.19 Volumeters are generally made of Plexiglas with a spout and come with a calibrated cylindrical collecting vessel. High clinical feasibility, however, may be hindered by the time investment to measure (filling, draining, cleaning), the potential excess size of a limb not fitting a volumeter, and the inability to measure the full limb to the groin.
It should be noted that a contraindication to using water displacement is the immersion of limbs with open wounds. A compelling reason for the importance of infectious disease precautions is due to the fact that those with lymphedema have a known compromise in their immune response with a greater risk of cellulitis.23 Another limitation in the use of volumeters for individuals with lower-extremity lymphedema is the possibility of an excessive size of the patient's leg. It is not unusual in some clinical settings to see patients with calf circumferences in excess of 120 cm, far exceeding the size of volumeters that are available commercially.
Circumferential Measurement by Tape Measure
Taking circumferential measurements at regular intervals with a nonelastic tape measure is the most widely used clinical method to determine the presence of lymphedema and assess volume changes when monitoring response to treatment. The best tape measures have several important attributes: are made of nonstretch material, are easily cleaned with alcohol swabs, and have clearly and easily discernible markings and an easily seen zero mark. The need for consistent tensioning of the tape can be addressed by the use of a tape measure, with a spring tension gauge at the zero end ensuring the exact same pull with each application. However, studies conducted on circumferential measurement without the use of this tension gauge have demonstrated good inter- (ICC = 0.97) and intrarater reliability (ICC = 0.92-0.99) in both upper- and lower-limb measurements.24 , 25
Reliable and reproducible measurements require a standardized positioning of the patient and establishment of reproducible landmarks for marking intervals of measurement. It is important to use a straight measure of intervals marked for measurement rather than a contoured laying on of the tape on the limb, as the contour of an abnormally shaped lymphedematous limb can change dramatically during treatment and lead to errors in subsequent markings of intervals for repeated measurement. Boards with a footplate provide this rigid straight method to mark intervals more consistently. Landmarks for the zero interval also improve the reliability of the resultant and subsequent measurements. In several studies, the landmark chosen is the malleoli,17–19 whereas in others,26 , 27 the heel is the landmark. In practice, the malleoli can be almost obliterated in the patient with lymphedema at evaluation so that a base of heel or distance from the floor (the footplate) to the bend of the ankle is least likely to change with treatment and should be used as the zero interval.28 The distance between intervals varies depending on the study; 4- and 10-cm intervals are reported.17 , 27 , 29 Both methods are reliable and valid and correlate highly with each other (r >0.99); however, the 4-cm method may better account for abnormal lobules in advanced lymphedema.24 , 29 Whichever interval is used for measurement, values are typically entered into an appropriate truncated cone formula to determine limb volume. The frustum or truncated cone formula is more accurate in assessing limb volume than a cylinder formula, as the limb is roughly the shape of a cone.30
The advantages of using a tape measure for volume measurement are cost (low) and accessibility (high) in the clinical setting. This measurement can also be done even if the patient has wounds or is unable to assume a standardized position for measurement by water displacement. When compared with the criterion standard water displacement, the validity is excellent (ICC = 0.93-0.98), except in grade 1 edema, where the correlation between measures is moderate (r = 0.45).17 , 26 , 27 Reliability is also excellent: test-retest reliability in a 1- to 2-week time frame was excellent (ICC = 0.94) and good (ICC = 0.82) in the long term; inter- and interrater reliability was both excellent (ICC = 0.89-0.99 and ICC = 0.82-99, respectively).19 Minimal ceiling or floor effects are present when measured with a tape measure; however, one study reported that when the leg volume difference is more than 11%, tape measurement overestimated the volume difference as compared with water displacement.17 One study examined the standard error of mean and determined this to approximately 84 mL or 0.64% of lower-leg volume.31 These sound psychometric properties and high clinical utility make this tool highly recommended by the EDGE Task Force.
The disadvantage of tape measurement method is time needed for multiple measurements and then calculation for comparison with contralateral “normal” limb or for comparison with pretreatment volumes. The time to calculate volume can be mitigated through the use of previously formatted spreadsheets such that simply entering circumferential values will render total volume and percent volume difference. Of clinical importance is the consideration that in lower-extremity lymphedema, the lymphatic compromise is often bilateral despite presentation of swelling in only one limb. Posttreatment measurements often demonstrate a volume reduction in what was thought to be a “normal” limb due to the focus in complete decongestive therapy on the proximal, intact lymphatic system. This is consistent with the physiological fact that there needs to be an increase of 20% to 30% in the normal interstitial volume before it is clinically apparent.32 Therefore, comparison over time may be a more clinically relevant measure.
Optoelectric volumetry, or perometery, is an assessment of limb volume that uses an array of infrared beams oriented via a square frame at right angles to each other. As the frame, tracking on a carriage, is passed over a limb in either a horizontal or vertical configuration, the limb volume is calculated using a computerized algorithm. The validity of optoelectric volumetry was established in comparison with water displacement and ranges from r = 0.97 to r = 0.99.33–35 Test-retest reliability is excellent with an ICC = 0.99.18 , 36 Intrarater reliability is reported as excellent, with an ICC of 0.99 or more.37 , 38 The repeated-measures coefficient of variation was reported as 0.13.36
The advantage of optoelectric volumetry is that a highly accurate limb volume can be calculated very quickly once the equipment is on and ready for use. For the commercially available perometer, additional benefits include optional compression garment measurement, as the software reports the actual circumference at the standardized landmarks used by German manufacturers for garment manufacturing.
The main disadvantages to the perometer being used in the clinical setting are the cost and size of the equipment. The equipment is large, requiring approximately half of the size of a typical treatment room. The purchase price in 2015 was US $16 000 to $26 000, with one primary manufacturer: Pero-System GmbH (Wuppertal, Germany). Whether to use a horizontal or a vertical system is dependent on the primary population to be measured. Although either unit can measure both upper extremity and lower extremity, a horizontal unit requires that the mid-frame be positioned at chair height for the lower extremity while the individual must bend over to measure the upper extremity in a vertical unit. The size of the frame limits the extent to which the unit can traverse proximally up the limb and reduces the volume calculation possible for the limb. Accuracy of the measurements depends on correct horizontal positioning of the limb and patients with limited range of motion may not be able to be correctly positioned.34 , 35 , 37 Newer optoelectric volumetry units, such as that designed by Skanlab, are being developed for clinical use.39 It is possible that other optoelectric volumeter units may be available commercially in the future.
Bioelectrical Impedance Analysis
Multifrequency BIA is a noninvasive assessment technique that uses a very small alternating current that is passed through tissue, creating a measure of impedance or resistance to flow of the current. The current moves through the path of least resistance in the tissues, measuring the resistance through the water content of the intracellular and extracellular portions of the soft tissue. Low-frequency current passes through the extracellular fluid, whereas high-frequency current passes through the intracellular fluid. BIA then measures both total resistance and the resistance of the extracellular fluid to quantify the impedance. This resistance is compared with an unaffected limb, creating an impedance ratio.22 Originally tested in women with breast cancer–related lymphedema, if this interlimb impedance ratio exceeds the mean ratio plus 3 standard deviations, a diagnosis of lymphedema is confirmed.40 , 41 Like other methods of volume assessment, preoperative values for comparison postsurgery are helpful for early diagnosis.40
Bioimpedance devices use 4 or 8 electrode arrays; the 8 electrode systems are considered to be more accurate.42 Recommendations for reproducibility included taking measurements at the same time with a constant ambient temperature and cleaning the sites with alcohol or wet wipes before standardized application of the electrodes.41 , 42 In a study comparing bioelectrical impedance values between individuals with a diagnosis of lymphedema via lymphoscintography and controls, BIA accurately identified those with lymphedema.43 Intratester reliability is ICC = 0.88 in a population with lymphedema due to filariasis.44 The predictive value of BIA was 53.2% in this same population.44 The sensitivity of BIA to monitor change was excellent in 2 studies: 100% sensitivity is reported in a population with lymphatic filariasis, and treatment differences compared with baseline were highly significant (P < .001) in patients with pedal edema.22 , 44
The most prominent advantage of BIA is that it can detect the onset of lymphedema before clinical signs of swelling become apparent.40 It can be completed in 5 to 15 minutes depending on the number of repeated measures made and is an accessible technology for preoperative values for reference in the postoperative period. A reference range has been established for the impedance ratio for the legs without pathology, allowing for criteria for the diagnosis of early lymphedema in the leg.41
The disadvantages of BIA are that it remains an assessment that, with the current bioelectrical impedance protocol that creates a ratio comparing the unaffected and affected limbs, is useful only for unilateral lymphedema risk.41 In most urogenital cancers, pelvic lymph node dissection and/or radiation therapy affect the lymphatic drainage patterns of both lower extremities even in a patient who presents with unilateral swelling. Another disadvantage of BIA is that it is useful primarily for the assessment of early stage (0-1) lymphedemas, as in the later stages of lymphedema, the extracellular fluid has been replaced to a large degree by fibrous tissue.45 When this has occurred, BIA is not helpful for diagnosis or monitoring of change over time. Finally, the electrodes are single use and therefore have a cost associated with each use.
Considerations in Measuring Limb Volume
Two cautionary issues arise when monitoring the lower limb at risk in urogenital cancer. First, there is a significant difference in volume assessments in the lower extremity when the entire limb is included in the measurements since the majority of swelling is often only below the knee.27 The length of the limb being measured, whether to the knee as is typical in water displacement or to the groin including the thigh, can also impact accuracy and interpretation. Specifically, as the amount of change in the smaller lower leg may be only a small percentage of the whole limb, the size of the thigh may mask the amount of change of the lower leg. Rather, using clinical judgment incorporating patient symptom report and clinician expertise, the measures used should be to the level of greatest involvement. If this is not amenable to water displacement, clinical judgment then determines that water displacement should not be used. However, if only the lower leg is involved, then this method may be appropriate. Ideally, it is clinically important to have measurements of the full thigh pretreatment because there is also a possibility of “fluid shift” into the proximal limb or genitals during treatment that must be recognized and addressed, and this is most easily accomplished via circumferential measurements with a tape measure.
The second consideration is the possibility of bilateral lower-limb involvement because this limits the usefulness of limb-to-limb comparisons. For this reason, it is essential that baseline measures are taken prior to medical intervention. The Prospective Surveillance Model developed for women with breast cancer includes baseline assessment and ongoing periodic monitoring.46 This model could easily be adopted for use in the urogenital cancer population. These baseline measures, then, would serve as a comparison for any changes in the lower limbs.
Ultrasound is not recommended by the Urogenital Cancer EDGE Task Force. The limited psychometric properties, in conjunction with decreased clinical utility, particularly cost and training, do not support its use for assessment of limb volume in this population. In a study examining the diagnostic validity of ultrasound, skin thickness was greater in the involved limb than in the noninvolved limb (P < .05) among women with breast cancer–related lymphedema,47 , 48 yet examining the ability to detect change over time was poor, as the change in skin thickness with a decrease in volume was only minimally correlated (r = 0.37).49 Furthermore, no studies examining reliability were found.
This topic of lower-limb lymphedema in the urogenital cancer population has not been studied to the extent seen in secondary lymphedema related to breast cancer. This resulted in far fewer studies in which the population of interest was available. The authors recommend that research be focused on accurately measuring lymphedema, whether directly or indirectly, in the urogenital cancer population. Additional research in the development of optoelectric volumetric tools is warranted in order for these tools to become more clinical useful. Furthermore, it is essential to develop reliable and valid clinical methods to measure genital lymphedema, and as this research need is significant, it should be prioritized. This literature search was completed in September 2015 and therefore any studies published thereafter with psychometric properties may not be included in this review. Newer studies may provide additional information to evaluate these measures, and the use of BIA is growing in use as measurement technique of lymphedema. We recommend these ratings be reviewed in approximately 5 years as new evidence becomes available. As lymphedema is a worldwide problem, limiting the search to the English language may have resulted in eliminating important research published elsewhere. All recommendations made by this Task Force are issued on the basis of the best available evidence at the time of analysis. The reader is encouraged to employ clinical judgment and expertise and to take into account patient values when implementing these recommendations.
This systematic review evaluated methods to measure lymphedema in the urogenital cancer population, focusing on lower-limb edema/lymphedema. Use of water displacement or circumferential measures with a tape measure was Highly Recommended by the Urogenital Cancer EDGE Task Force. These measures have sound psychometric properties and high clinical feasibility. Further research is needed in valid and reliable methods to measure genital lymphedema.
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edema; limb volume; measurement; psychometrics; urogenital neoplasms
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