Cancers of the head and neck (HNC) involve the oral cavity, pharynx, larynx, paranasal sinuses, nasal cavity, salivary glands, upper esophagus, face, associated musculature, and/or bone and some thyroid cancers.1 Head and neck cancer represents 3% of all cancer survivors in the United States and is considered an understudied tumor type.2 The 5-year relative survival rate of these cancers widely varies—94% (lip cancer), 74% (salivary gland), and 30% (hypopharynx, and “other” cancers of the oral cavity and pharynx)2 with approximately 291,108 people living with oral cavity and pharyngeal cancers in the United States in 20123- likely an underestimate since laryngeal, thyroid, and upper esophageal cancers are also head and neck cancers.3,4 Despite the rarity of HNC, disability and other side effects are highly prevalent. Lymphedema is known to affect the majority of HNC survivors (60-80%) affecting external structures (eg, outward and obvious swelling of the neck, head, and face), internal structures (eg, tongue, oral cavity, pharynx, hypopharynx, larynx, trachea, and esophagus), or a combination of both.5,6 Head and neck cancer survivors usually have one or multiple treatment modalities. For example, tumor and lymph node resection and/or radiation, chemotherapy, or combined chemotherapy and radiation (CCR).7,8 These treatments can be a grueling experience with serious side effects (eg, mucositis, cachexia, fatigue, oral and non-oral pain) that may require feeding tube placement.9
Location of the tumor, tumor and lymph node resection, radiation, and multiple modality treatment are all associated with lymphedema of the head and neck.5 Other posttreatment factors such as muscle guarding, abnormal posture, and reduced movement in the affected areas may also contribute to lymphedema among HNC survivors.10 Lymphedema, left untreated, can have serious consequences resulting in risk for recurrent infection such as cellulitis, and interference with the ability to breathe, swallow, and/or speak—key functions of life.6
The 5-year relative survival rate from HNC, particularly for those with human papillomavirus (HPV) positive tumors, is improving. Survival rates (relative and absolute) are high. For example, survival rates for oral cavity and pharyngeal tumors are 62.7% and for laryngeal cancers, 60%. With increased survival, it stands to reason that more HNC survivors will be living with long-term cancer-related lymphedema.6,12 Head and neck cancer survivors diagnosed with lymphedema are commonly referred to physical therapy for lymphedema management.13,14 Complete assessment of lymphedema involves patient subjective complaints, physical examination (ie, pitting, tissue texture), and objective tests and measures.15-17 Reliable and valid measures are necessary for clinicians to accurately assess and document patient progress and guide clinical decision-making.
This systematic review is part of the Evaluation Database to Guide Effectiveness (EDGE) activities of the American Physical Therapy Association Oncology Section's Head and Neck Cancer Task Force. The purpose of this systematic review is to identify and provide recommendations of clinically feasible and relevant objective tests and measures of edema for HNC survivors with cancer-related lymphedema.
DATA & METHODS
The authors registered this systematic review on PROSPERO (CRD42013004898). The search was limited only to studies that report on measurement of edema due to cancer treatment-related lymphedema of the head and neck. Because little research exists on concerns of HNC survivors that falls within the scope of physical therapy practice, we placed no limits on publication dates or level of evidence. We conducted a search of literature databases (PubMed, PEDro, EBSCO Host, Medline, PsycInfo, and Cochrane Database) using the following key words in all combinations: edema, human, lymphedema, cancer, head, neck, radiation, radiotherapy, surgery, neck dissection, face, measurement, outcome, outcome measure, radiation fibrosis, lymphostasis, inflammation, reliability, and validity. Articles were limited to studies on humans and published in English. Duplicates were removed and abstracts for all citations were screened to determine if they were to be included in the final review. Figure 1 illustrates the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) process used for the literature search.
Two investigators (AMF and BAS) independently completed a search of the literature using the databases and personal files of published articles not included in the literature databases as mentioned earlier in June 2014. This provided verification of the search results. The investigators then independently reviewed the abstracts of the search results and eliminated non-relevant articles based on the predetermined inclusion criteria (English language, any date of publication, any level of evidence) and exclusion criteria (no requirement of a physician prescription or performance of a medical procedure for measuring edema, nonhuman sample, quality of life study). The measures of edema identified by the authors were divided between reviewers, who independently retrieved relevant studies and full-text articles for each measure to assess clinical feasibility, psychometric properties, and relevance to the HNC patient population. The primary reviewer completed the HNC Task Force Outcome Measure Rating Scale Form (Table 1) for each assigned measure. The risk of bias of measure assessment was addressed by ensuring a secondary review for all measures. In the case of a discrepancy in rating between reviewers, two other investigators were available to evaluate the reviews and determine the decision outcome, along with the other two investigators, until total agreement was reached. Outcome measure recommendations were agreed upon using the EDGE criteria resulting in an ordinal score with anchors at 1 (measure is not recommended) and 4 (measure is highly recommended) (see Table 1).18
Using our keywords, we identified 25,007 records. All duplicates were removed which resulted in 11,337 articles. Eighty-six outcome measures of lymphedema were identified; 40 were patient reported outcomes (PRO) (represented in 141 articles) and the remainder were clinical measures (represented in 254 articles). We excluded 46 measures which had only one article addressing the measure. Using the remaining articles, the investigators generated a list of 12 measures of edema for HNC treatment-related lymphedema. Of these clinical measures, only 7 represented measurements of external edema for lymphedema of the head and neck that can be performed by physical therapists: real-time ultrasound, 3-dimensional (3D) laser scanning, tissue dielectric constant (TDC) method, M.D. Anderson Cancer Center - head and neck lymphedema rating scale (MDACC-HNLRS), and the ALOHA method (circumferential volume revised for head and neck), frustum volume estimation, and disk model method. One hundred thirty-nine references were included in the review (see Figure 1 and Table 1).
“Highly Recommended” and “Recommended” Edema Outcome Measures
In order to reach this level of recommendation, the measure must have evidence supporting excellent psychometric properties and clinical utility. The measure should also have been tested in the HNC population. Of the 6 measures, none reached the level of “highly recommended” or “recommended,” per the requirements outlined in Figure 2.
“Unable to recommend at this time” Edema Outcome Measures
This recommendation has two levels depending on whether the measure has been used in the HNC patient population (2A) or not (2B). Four types of measures reached this level of recommendation. Three of these use technological devices to measure external edema—ultrasound, 3D scanning, and TDC. The final type is standardized tape measurement of the head, neck, and face. Included in this final type are two different approaches—the MDACC-HNLRS and the ALOHA tape measurement system. All have been used in the HNC population.
Real-time ultrasound measures skin-to-bone distance, skin thickness, subcutaneous thickness, and/or resistance to compression. Measurement of skin to bone distance at the mandibular ramus, angle and hyoid using a 7.5 MHz linear transducer was found to be reliable in healthy individuals (intraclass correlation coefficients ICC, ranged from 0.88 to 0.97).14 Skin thickness (r = 0.95) and subcutaneous thickness (r = 0.84) have been shown to be strongly correlated with duration of lymphedema in women with breast cancer-related lymphedema.19 At the time of this writing and to the best of our knowledge, no studies have formally investigated the responsiveness of ultrasound as a measure of edema among those with HNC-related lymphedema. However, one study showed a significant reduction in skin-to-bone distance after patients with HNC-related lymphedema received a course of manual lymphatic drainage and compression therapy.14 Significant differences in skin thickness were found in patients who received systemic enzyme therapy after undergoing bimaxillary orthognathic surgery compared to those who did not receive systemic enzyme therapy.20
Three-dimensional scanning is a more recent application in its use for edema measurement. It has been used in a variety of industries—engineering where it is used for design and building projects;21,22 forensics where it is used to estimate size, volume, and topography of missing body parts;23,24 manufacturing where it is used for machining;25,26 and dentistry where it is used in the creation of dental implants and dentures.27,28 Threedimensional scanning uses laser technology to scan the body part to be measured. It is a noninvasive approach with no radiation exposure and excellent reproducibility, with an error of less than one tenth of a millimeter.29-31 However, Harrison et al reported a measurement error range between 0.3-4.0 cm3 largely attributed to changes in positioning.32 The sensitivity33 and reliability29-40 of this method of edema measurement are high. Ramos and colleagues33 report that 3D imaging is sensitive, reproducible, and significant in detecting change in those with breast cancer-related lymphedema with initial volumes of 500 mL or less. The mean error of measurement for volume measured using 3D imaging has been found to be within 3.5%.39 Kau et al40 measured facial morphology in 473 male and female subjects using this technology. The average linear distance among male subjects ranged from -6.30 to 4.44 mm, with similar measurements among females ranging from -6.32 to 4.25 mm.40 Together, these studies provide reference values for comparison for future studies. Limited research33,39,40 using this method in the HNC survivor population exists at this time. However, this method allows one to measure any linear distance from any point to another in the affected and unaffected areas.
Like the 3D scanning technique, the TDC has also been used in health research and other industries. The Moisture Meter D (Delfin Technologies, Kuopio, Finland), is the only TDC device that has been tested with HNC survivors to measure cancerrelated lymphedema. Inter-observer reliability, measured by the ICC has been found to be 0.973 in previous research.41-43 Internal consistency has not been reported nor has the measurement error for the head and neck. The TDC device measures physiologic properties of biological fluid to a depth of between 0.5 mm - 5 mm for the ventral forearm and 2.5 mm on the lateral thorax. These depths not only vary by body location but also depend on the diameter of the probe used for TDC.41 Recently, the TDC has been tested on the forehead and just below the maxilla (cheek) to measure the TDC up to a depth of 0.5 - 2.5 mm, but the thickness of the skin was a mediator in the measurement. This means that as tissue thickness increases in the forehead, the TDC value is reduced, but the opposite is true for the maxillary TDC measurement. However, in general, as tissue thickness increases, so does the TDC value indicating increased water content.44 Only a few studies have used this method with HNC survivors, but it has not yet been tested for safety, efficacy, diagnostic reliability, and validity with large samples. Nixon et al45 report interrater reliability as 0.97. They also report that the TDC, as measured by the Moisture Meter D, was able to discriminate between HNC survivors and healthy controls (t = 8.97, p < 0.001). The TDC was also correlated with linear tape measurements of the head and neck area (rho = 0.37-0.38), but not with the rating scale used by the MDACC-HNLRS. This study used a small sample size of 40—20 HNC survivors and 20 healthy controls.43 At the time of the writing of this paper, this device is experimental in the United States in terms of its application in assessing edema of the head and neck. Unfortunately, none of the studies examined for this review considered obesity or tissue fibrosis as possibly leading to inaccurate estimates of fluid in the head and neck.
The tape measurements are based on dental and maxillofacial surgery measurement standards first described by Gabka et al46 and later modified by Schultze-Mosgau et al.47,48 Both were further adapted by Smith and Lewin to include neck measurements used in the MDACC-HNLRS.17 The facial measures rely on the use of bony landmarks of the face and head.17,43,44 Both MDACC-HNLRS and the ALOHA approach use linear distance measures. The MDACC-HNLRS uses 12 measures adapted from Gabka et al.46 Two are point-to-point measures (mandibular angle to angle and tragus to tragus), 7 are facial measures (tragus to mental protuberance; tragus to mouth angle; mandibular angle to nasal wing; mandibular angle to medial canthus; mandibular angle to lateral canthus; mental protuberance to medial canthus; mandibular angle to mental protuberance), and 3 are circumferential neck measures (superior neck immediately beneath the mandible; medial neck midway between the superior and inferior neck; inferior neck at the base of the neck).17,46 The ALOHA tape measurements utilize one point-to-point measure (ear to ear beginning at the inferior ear lobe/face junction of the left and right meeting at a point 8 cm inferior to the lower lip); 3 circumferential measures (lower neck circumference at the base of the neck; upper neck circumference inferior to the mandible; length from lip to lower neck circumference along the midline inferior lower lip to lower neck circumference). Purcell et al43 compared 3 measurement methods—MDACC-HNLRS, ALOHA, and TDC alone. The ALOHA trial showed high interrater reliability for 3 tape measures with ICCs ranging from 0.948 (ear to ear length), 0.969 (upper neck circumference) and 0.979 (lower neck circumference).43 The only tape measurement found not to have high interrater reliability was the lip to lower neck circumference length (ICC = 0.420).43 Unlike the TDC, tape measures did not significantly discriminate between HNC survivors with lymphedema and healthy controls.43 However, the authors recommend the tape measures as sensitive enough to measure within-person change over time, but did not provide evidence to support this claim.43 Moreover, from a practical perspective, tape measurement takes a great deal of time to perform, making it difficult to measure irregularly shaped parts of the face and head such as the edema in the mandibular, auricular, nasal, orbital and submandibular areas. Table 2 provides a summary of the psychometric properties of these measures.
“Not Recommended” Edema Outcomes Measures
The remaining two measurements—frustum and disk model methods—merited a score of “not recommended.” This means that poor psychometrics and lack of clinical utility exists for the frustum and disk model methods. Both of these edema measures were tested together in the studies we examined; however, it is important to note that each is a distinct method. The frustum method is an ancient method used to estimate the volume of multi-sided pyramidal shapes. A frustum is a geometric solid volume measurement of a cone or pyramidal structure and is created by at least two planes that bisect one another to form a side of a cone. In contrast, the disk method relies on the sum of multiple circumferential measures of a cone. Both methods are ideal for conical measures, and therefore, have been limited to use in the extremities.48,49 An exception to this is one study that used a sample of 4 patients with head and neck lymphedema, in which the frustum method was calculated based on circumferential tape measurements of the head.50 The frustum and disk model methods have also been used to measure volume of the prostate—another irregularly shaped body part. The frustum method was found to underestimate prostate volume by 50% when compared to planimetry and overestimated volume compared to ultrasound guided MRI.45 While these methods are useful for the extremities, only the frustum method has been used on a small sample of HNC survivors50 at the time of this writing. Unfortunately, no psychometric data are reported for the HNC patient population using these measures (see Table 2).
While smoking and/or alcohol abuse are common causes of HNC,1 specific types of HPV cause nearly 32% of all HNC cases and this incidence is expected to rise.12 With this growth, we expect that physical therapists will experience increased referrals for patients with HNC. In addition to lymphedema, HNC survivors undergoing treatment will have reduced dietary intake, with 37% to 68% experiencing moderate to severe pain, impaired swallowing, xerostomia, taste, and hoarseness.52 Conical measures using circumferential measures or formulae dependent on circumferential measures (eg, frustum, disk model methods) are easy to use to measure edema of the extremities, but they do not adequately measure edema in the head and neck. These methods may underestimate volume of the head and neck.51 Aside from surgical anatomy changes and associated side effects, the addition of side effects associated with chemotherapy, radiation, or CCR increases the risk of lymphedema of any of the structures targeted by cancer treatment. For example, radiation-induced tissue fibrosis will include damage to the remaining lymphatic structures in the treated area.54
Subjective information through self-reports such as heaviness, tightness, and firmness5,6 along with objective information provided by clinical measurement of lymphedema can provide information to determine successful outcomes when treating HNC survivors. Lymphedema is a multi-faceted diagnosis based on the presence or absence of skin integrity, color, edema, pitting, positive Stemmer's sign, and malformations associated with lymphostasis and infection.15 Therefore, using edema measurement as a singular indicator of lymphedema can be misleading in determining the severity of the lymphedema.16,55 However, in the head, face, and neck, edema drastically changes one's appearance and may impair the ability to breathe, swallow, and vocalize, making external measures of edema a crucial part of any physical therapy examination, evaluation, and assessment of the HNC survivor. It is important that physical therapists treating the HNC survivor with lymphedema have reliable and valid measures of edema that are clinically feasible and have realistic and reasonable associated costs. While there are also internal measures of lymphedema, these are invasive and require technical procedures that fall outside of the scope of physical therapist practice. For example, a bronchoscopy is performed by an otolaryngologist to assess internal swelling as well as check for cancer recurrence in the oropharyngeal cavity, as Deng and colleagues have done. Bronchoscopy is not risk-free. These risks include aspiration, vocal cord damage, bleeding, oxygen desaturation, bronchospasm, fever, pneumonia, pneumothorax, and death.56,57 Physical therapists specializing in HNC would benefit from having well-formed relationships with physician or speech therapy practitioners to take advantage of information resulting from imaging procedures outside the PT scope of practice. Additional measurements could be taken and internal and external volume could then, hypothetically, be calculated. Three-dimensional scanning, ultrasound, and TDC can be performed by physical therapists; however, each require additional training on the use and application of these methods. Three-dimensional scanning has a steep learning curve because it requires that the user know how to use the scanner and requires multiple images to render a 3D image. The software to create these images is complex and difficult to learn. Further, the cost of a 3D scanner, software and software training is cost-prohibitive for the average clinical setting. Real-time ultrasound, on the other hand, is increasingly utilized in physical therapy clinics and those who already use it for evaluation of treatment of patients (such as urinary incontinence or adhesive capsulitis) may find it easy to use in the HNC patient population. Finally, TDC appears to be the easiest to use, set-up, and interpret.
Quantifying edema reduction is crucial to gauge the effect of treatment for lymphedema in the head and neck. It presents a unique measurement challenge in effectively treating HNC survivors. Edema measurement will fulfill new Medicare outcomes documentation requirements to demonstrate reduction in volume due to external lymphedema. At this point, there is no gold standard to measure edema in the head and neck. Common practice involves linear distances of the face and circumferential measures of the neck—such as those used in the MDACC-HNLRS and ALOHA methods. However, neither of these methods actually measure volume but provide a way to document reduction in linear distance that is reasonably expected to reflect a reduction in volume in response to treatment. The advantage of the linear distances used in these measures is that clinically speaking the baseline of these measures could be measured using diagnostic MRI or CT scan. However, this approach involves the cooperation of physicians—particularly radiologists—and is not typically measured as part of clinical standards of care. Another advantage of the MDACC-HNLRS and ALOHA methods is that both provide a systematic way to measure edema. The ALOHA method also incorporates measurement of the TDC and, similar to the MDACC-HNLRS, also uses tape measurements and classification of HNC lymphedema characteristics. These approaches are clinically feasible, cost-effective, and not time-intensive. The linear measurements are estimated by the authors to take approximately 5 minutes to measure by clinicians experienced with HNC survivors, making them not time intensive. However, the inclusion of the TDC increases the time to complete the measurement and, in total (linear and TDC measurement), we estimate these could take up to 10 minutes. Ten minutes could take up one third of the time to evaluate or treat a non-complex patient, even more time may be required if the physical therapist needs to re-measure. At this point though, TDC is not commonly used clinically and is not likely to be found in the average clinic.
The techniques of ultrasound, 3D scanning, and TDC methods hold great promise for clinical translation but all need more research investigating their psychometric properties of reliability and validity, sensitivity to change, and references for comparison. All 3 are used to measure external edema and, while none addresses the measurement of internal edema, they are noninvasive and not dependent on a skill set possessed only by physicians. Like MRI and CT-scanning methods, 3D laser scanning can precisely measure external lymphedema and does not require a medical referral. The disadvantage is that the entire volume of the head and neck region is assumed to be included in the overall volume measure. To illustrate, it assumes that the scanned area is a solid with no “empty” spaces such as the oral cavity, sinuses, pharynx, larynx, and upper esophagus. Of these 3 methods dependent on the use of technology, 3D scanning is prohibitively expensive and presents a steep learning curve for the physical therapist. In addition to the 3D laser scanner (of which there are several types to choose), the clinic will also need to purchase 3D computer software to measure volume. The computer programs are complicated and require intensive training. Other costs associated with the use of the 3D scanner include software training, service agreements, software updates, repair costs, and costs for personnel to take the images and render them usable in 3D software.
In contrast, the TDC is a small hand-held device that provides fast and readily available measurements. The TDC measures the electrical properties of lymphatic fluid—not necessarily edema like 3D scanning—but it is comparable to the MDACC-HNLRS and ALOHA systems. Likewise, ultrasound holds promise and further research is warranted. We caution that the 3D scanners, real-time ultrasound, and TDC devices may be cost-prohibitive for a clinic to purchase.
Measurement of head and neck lymphedema poses many challenges to physical therapists. Methods that are clinically realistic are limited and few have had in-depth testing with patients with HNC. Head and neck cancer is a rare tumor type and patients tend to be very sick during active treatment, making it difficult to recruit and retain large samples for research. The MDACC-HNLRS and the ALOHA measurement systems are the best available and feasible measures for use in the physical therapy clinic. Collected prospectively and across clinics, these measurement systems may provide important data for future research and comparability across clinics.
While we focused on measurement of external edema for the HNC survivor with cancer-related lymphedema, it is clear that much more research needs to be conducted to address the complex cluster of issues typical of lymphedema. Future research will address this through the review of PROs related to QOL and lymphedema.
Measurement of lymphedema of the head and neck is in its infancy. Few methods exist to calculate volume and/or physiological properties that characterize lymphedema of the head and neck. Volume assessment using tape measures and specific landmarks are the most commonly used method currently, but other methods such as 3D scanning, ultrasound, and TDC hold great promise. However, because of the lack of good psychometric properties or clinical utility, no outcome measures for objectively quantifying external edema for the HNC population can be recommended at this time. The future development and application of these devices to measure edema in HNC survivors with lymphedema merits systematic and comparative research to evaluate measurement properties such as reliability, validity, sensitivity to change, and normative values. Much research needs to be conducted to develop and compare a variety of methods for edema of the head and neck. We recommend that physical therapists fully weigh the advantages and disadvantages of any measure of edema while treating HNC survivors.
No funding was available for this project. All member efforts were on a volunteer basis. We wish to thank Elyse Bloomfield and Mariesa Gonzalez (students in the Northeastern University DPT program) for assisting with downloading and screening of abstracts.
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