Introduction
The sentinel lymph node (LN) is the first LN to which malignant cells are most likely to spread from a primary tumor.1 Therefore, assessment of the sentinel LN is an integral part of tumor staging, because the absence or presence of LN metastasis may affect prognosis and treatment.2 Palpation and caliper measurement of peripheral LNs are frequently used to evaluate their size. However, prior studies3,4 reveal that palpation is an insensitive detection method of LN metastasis. In small animal practice, microscopic examination of cells collected through fine-needle aspiration (FNA) of peripheral LNs commonly complements palpation. Fine-needle aspiration is minimally invasive, cost-effective, and highly sensitive and specific for the diagnosis of LN lesions.5,6 However, depending on LN location and tumor type, multiple samples may be required, potentially increasing the risk of complications and cost of the FNA procedure,7 and FNA may yield nondiagnostic samples.8
Conventional (B-mode) and Doppler ultrasonography have been used to evaluate the size, shape, echogenicity, margination, texture, vasculature distribution, and perfusion of peripheral LNs. A lymph node’s fibrotic capsule often appears thin and hyperechoic; its hilum as numerous acoustic interfaces because the hilum is a small, flat or concave area that consists of a supplying artery, veins, nerves, efferent lymphatic vessels, and a small amount of fat; its cortex as an isoechoic to hypoechoic peripheral region that consists of lymphatic follicles with a large number of lymphocytes; and its medulla as a hyperechoic central region with a less organized and less cellular structure that contains the medullary cord and sinus.9–11 Yet results of some studies12–14 that included an attempt to characterize malignant LNs by use of ultrasonography are inconclusive. Therefore, criteria for predicting LN malignancy by ultrasonography are currently unreliable.
Elastography, which incorporates ultrasonography, is a relatively new method to evaluate the elastic properties and stiffness of tissues. One form of elastography, strain elastography, can be used to estimate relative tissue elasticity by comparing local tissue displacement before and after the application of a manual compressive force. However, because pressure is manually applied with an ultrasound transducer, strain elastography cannot be used to quantitatively evaluate tissue stiffness and tissue displacement can vary greatly on the basis of the pressure generated by the ultrasonographer. The other form, shear-wave elastography (SWE), can be used to estimate tissue elasticity (elastic modulus) by measuring the speed of a shear wave that is generated by an ultrasound transducer. The transducer generates acoustic radiation forces that propagate transversely and displace particles in tissues. Shear-wave elastography estimates shear-wave velocity (SWV), which is then used to calculate Young (elastic) modulus on the basis of the formula E = 3pVs2, where E = Young modulus (in kPa), P = tissue density (in kg/m3), and Vs = SWV (in m/s). Therefore, by measuring SWV, SWE can quantitatively assess soft-tissue elasticity.15,16
In human medicine, SWE has been used to noninvasively evaluate changes in the elastic properties of tissues of various organs associated with specific pathological or physiologic processes.15 The results of several studies17–22 indicate that the elasticity of malignant lesions is higher than that of benign lesions, suggesting that the use of SWE combined with B-mode ultrasonography may improve diagnostic accuracy. Also, malignant LNs had higher SWVs, and maximum SWV had higher sensitivity and negative predictive value, compared with B-mode ultrasonographic features (short-to-long axis ratio and presence of calcification or cysts), for predicting malignancy. Because infiltration and dense packing of neoplastic cells decrease tissue elasticity, SWE successfully differentiates malignant from benign nodules in thyroid gland and breast tissues and cervical LNs.17,18 Similarly, hepatic fibrosis causes the liver to become stiffer than normal.23,24
Moreover, several studies25–29 of dogs reveal the usefulness of SWE in the evaluation of the mammary glands, liver, spleen, and skeletal muscles. In one of these studies,26 SWE was performed on the axillary, mandibular, medial retropharyngeal, and superficial inguinal LNs in healthy Beagles. However, to the authors’ knowledge, no study has been published that reports the SWVs of all superficial and medial retropharyngeal LNs and the differences in SWVs among LNs in relation to the scanning plane and position and size of the region of interest (ROI).
Therefore, the objectives of the study reported here were to determine the SWVs of various superficial LNs of healthy dogs; define differences in SWVs among the LNs; evaluate the differences in SWV among LNs in relation to the scanning plane and position and size of the ROI; and determine intra- and interobserver agreement for SWVs.
Materials and Methods
Animals
Included in this study were 11 Beagles (sexually intact male, n = 8; sexually intact female, 2; spayed female, 1) that had a mean age of 5.7 years (range, 3 to 8 years) and a mean body weight of 10.5 kg (range, 9.3 to 12.3 kg). No dog had a history of local or systemic disease and all were determined to be healthy at the time of the study on the basis of results of a physical examination, CBC, serum biochemical analysis, echocardiography, and abdominal ultrasonography. Cells were aspirated with ultrasound guidance and examined microscopically from all ultrasonographically examined LNs except for the medial retropharyngeal LN following measurement of SWVs. Lymph nodes were considered normal when microscopic examination of aspirated cells revealed many small lymphocytes, with only a few plasma cells and intermediate and large lymphocytes. All dogs were fasted for at least 12 hours (maximum of 24 hours) with water available ad libitum before SWE was performed. The study was approved by the Institutional Animal Care and Use Committee at Konkuk University (approval Nos. KU20117 and KU20090).
Measurement of SWV
Shear-wave elastography was performed with a 10-MHz linear array transducer (PLT-1005BT; Canon Medical Systems) and an ultrasound machine (Aplio 500 and Aplio a; Canon Medical Systems) that had software for SWE. Some dogs were lightly sedated with medetomidine hydrochloride (Domitor; maximum dose of 40 µg/kg, IM) to minimize movement artifacts. Bilateral superficial and medial retropharyngeal LNs were evaluated for each dog, thereby yielding 132 LN examinations. Each LN was examined with SWE in sagittal and transverse planes sequentially. The hair over the target region was clipped, and the dogs were positioned in dorsal recumbency with the neck slightly extended for imaging of the mandibular and medial retropharyngeal LNs, the forelimb slightly extended caudally for imaging of the superficial cervical LN, the forelimb slightly abducted for imaging of the axillary LN, the hind limb flexed and abducted for imaging of the superficial inguinal LN, and the hind limb positioned slightly perpendicular to the body for imaging of the popliteal LN (Figure 1). A thick layer of ultrasound acoustic gel was applied to the target area to improve skin contact and minimize the pressure on the transducer exerted by the ultrasonographer. The depth from the skin surface to the LN was recorded for each LN.
Photographs of a healthy adult Beagle positioned in dorsal recumbency for shear-wave elastography (SWE) of various peripheral lymph nodes (LNs). A—For examination of the mandibular and medial retropharyngeal LNs, the neck was slightly extended prior to placement of the ultrasound transducer. B—For examination of the superficial cervical LN, the forelimb was slightly extended caudally prior to transducer placement. C—For examination of the axillary LN, the forelimb was slightly abducted prior to transducer placement. D—For examination of the superficial inguinal LN, the hind limb was flexed and abducted prior to transducer placement. E—For examination of the popliteal LN, the hind limb was positioned slightly perpendicular to the body prior to transducer placement.
Citation: American Journal of Veterinary Research 82, 12; 10.2460/ajvr.82.12.981
Data reliability was determined by the proper propagation and color maps.29 When the contour lines were regularly parallel to each other and nearly straight on the propagation map, data reliability was considered high, and when the contour lines were irregularly distorted and chaotic on the propagation map, data reliability was considered low (Figure 2). Additionally, the color map displayed the SWV (range, 0.5 to 6.5 m/s) in a gradual series of colors. As the elastic modulus increased, the color map was displayed in an ascending order of blue, green, yellow, and red. Regions that were not color coded on the color map indicated the absence of a shear wave; therefore, SWV should not be measured in those regions.
Shear-wave elastographic images of the color map (A and C) and propagation map (B and D) obtained for a mandibular LN from a healthy adult Beagle used for shear-wave velocity (SWV) determination. The parallel contour lines (B; yellow arrows) indicate high reliability of the data, and the irregularly distorted and chaotic contour lines (D; red arrow) indicate low reliability of the data. The regions that are not color coded (C; asterisk) indicate the absence of a shear wave. T1, T2, and T3 denote the regions of interest (ROIs) that were used for SWV determination.
Citation: American Journal of Veterinary Research 82, 12; 10.2460/ajvr.82.12.981
The ROI was placed in 2 or 3 positions of high data reliability to measure SWV. Measurements at the peripheral and central positions of each ROI referred to those obtained in the peripheral relatively hypoechoic cortical portion and central relatively hyperechoic medullary portion of each LN, respectively, and measurement of the entire position referred to that of the cortical and medullary portions combined. The size of the ROI was set at 1 X 1 mm for measurement of the peripheral and central positions and set to the maximum size that did not exceed the size of the LN for measurement of the entire position. In the sagittal scanning plane, the ROI was placed on the peripheral, central, and entire positions of the LN, and in the transverse scanning plane, ROI was placed on the peripheral and entire positions (Figure 3). At least 3 SWV values were obtained for each measurement. The depth (skin surface to LN, in cm) of each measurement was recorded.
Shear-wave elastographic images of the color (left panels) and propagation (right panels) maps obtained from a sagittal scanning plane for a superficial cervical LN of a healthy adult Beagle used for SWV determination. A—Three 1 X 1-mm ROIs for the peripheral position of the LN. B—Three 1 X 1-mm ROIs for the central position of the LN. C—Three ROIs for the entire position of the LN. T1, T2, and T3 denote the 3 ROIs that were used for SWV determination.
Citation: American Journal of Veterinary Research 82, 12; 10.2460/ajvr.82.12.981
To evaluate intraobserver reliability, intraday (at least a 6-hour interval between examinations) and interday (at least a 1-week interval between examinations) assessments of SWVs for each LN were performed by 1 investigator (Y-RK). To evaluate interobserver reliability, assessments of SWVs of each LN were performed by 2 other investigators (S-HL and I-MS). The 3 investigators were trained in ultrasonography. Intraclass correlation coefficients were used to describe intra- and interobserver reliability. An intraclass correlation coefficient of < 0.4 indicated poor reliability, 0.41 to 0.6 moderate reliability, 0.61 to 0.79 good reliability, and > 0.8 excellent reliability.
Statistical analyses
Continuous data were confirmed to be normally distributed on the basis of visual interpretation of probability plots (raw data vs 95% CIs). All data were reported as mean ± SD. The independent sample t test was used to assess differences in SWVs for each LN based on the position and size of the ROI and scanning planes (sagittal vs transverse) and to assess differences among LNs. All statistical tests were performed with commercially available software (SPSS version 25.0; IBM Corp). Values of P < 0.05 were considered significant.
Results
The mandibular LNs were the most superficial (mean ± SD depth, 0.74 ± 0.15 cm), and the medial retropharyngeal LNs were the deepest (1.30 ± 0.22 cm). The distances from the skin surface to each of the other LNs were as follows: axillary, 1.24 ± 0.63; superficial cervical, 1.16 ± 0.34; popliteal, 0.97 ± 0.25; and superficial inguinal, 0.81 ± 0.24.
The SWVs of each LN acquired from the sagittal and transverse scanning planes are summarized (Tables 1 and 2). For each LN, regardless of scanning plane, SWVs did not significantly differ between positions (peripheral vs central, central vs entire, and peripheral vs entire). The SWVs of all LNs that were acquired in the sagittal scanning plane were significantly higher (P < 0.001 for mandibular, medial retropharyngeal, superficial cervical, and superficial inguinal LNs; P < 0.019 for popliteal LNs), compared with the SWVs that were acquired in the transverse scanning plane (Figure 4). The SWV of the axillary LN could not be measured from the transverse scanning plane because the ultrasound transducer’s field of view was large (approx 58 mm).
Mean ± SD shear-wave velocities (SWVs) (m/s) acquired from the sagittal scanning plane of a region of interest (ROI) for each of 3 lymph node (LN) positions (periphery [P], center [C], and entire [E]) for various LNs of 11 healthy adult Beagles.
| LN | Position of ROI | P value* | ||||
|---|---|---|---|---|---|---|
| P | C | E | P vs C | P vs E | C vs E | |
| Mandibular | 1.83 ± 0.20 | 1.84 ± 0.21 | 1.85 ± 0.18 | 0.895 | 0.744 | 0.856 |
| Medial retropharyngeal | 1.72 ± 0.20 | 1.74 ± 0.20 | 1.74 ± 0.19 | 0.767 | 0.686 | 0.918 |
| Superficial cervical | 1.61 ± 0.18 | 1.62 ± 0.17 | 1.63 ± 0.17 | 0.853 | 0.608 | 0.740 |
| Axillary | 1.38 ± 0.21 | 1.36 ± 0.19 | 1.37 ± 0.22 | 0.702 | 0.843 | 0.868 |
| Superficial inguinal | 1.60 ± 0.16 | 1.62 ± 0.15 | 1.61 ± 0.18 | 0.657 | 0.787 | 0.887 |
| Popliteal | 1.53 ± 0.14 | 1.53 ± 0.13 | 1.57 ± 0.14 | 0.965 | 0.448 | 0.408 |
Values of P < 0.05 were considered significant.
Mean ± SD SWVs (m/s) acquired from the transverse scanning plane of an ROI for each of 2 LN positions for various LNs of the dogs of Table 1.
| LN | Position of ROI | P value* | |
|---|---|---|---|
| P | E | P vs E | |
| Mandibular | 1.55 ± 0.18 | 1.54 ± 0.17 | 0.926 |
| Medial retropharyngeal | 1.48 ± 0.13 | 1.50 ± 0.17 | 0.671 |
| Superficial cervical | 1.33 ± 0.12 | 1.35 ± 0.12 | 0.704 |
| Superficial inguinal | 1.30 ± 0.18 | 1.34 ± 0.17 | 0.469 |
| Popliteal | 1.44 ± 0.29 | 1.44 ± 0.18 | 0.605 |
See Table 1 for key.
Box-and-whisker plots of the SWVs for the mandibular (M), medial retropharyngeal (MRP), superficial cervical (SC), superficial inguinal (SI), and popliteal (P) LNs acquired through SWE in sagittal and transverse scanning planes for 11 healthy Beagles. The horizontal line within each box represents the median, boxes represent interquartile (25th to 75th percentile) range, and whiskers indicate the maximum and minimum values. Brackets denote comparison groups. *P < 0.05. †P < 0.001.
Citation: American Journal of Veterinary Research 82, 12; 10.2460/ajvr.82.12.981
From the sagittal scanning plane, SWV for the axillary LN was significantly lower, compared with that for the other LNs (P < 0.001 for mandibular, medial retropharyngeal, superficial cervical, and superficial inguinal LNs; P = 0.001 for the popliteal LN). The SWV of the mandibular LN was significantly (P < 0.001) higher, compared with that of the other LNs except for the medial retropharyngeal LNs. The SWV for the medial retropharyngeal LN was significantly higher, compared with that for the superficial cervical, axillary, superficial inguinal, and popliteal LNs (P < 0.001 for superficial cervical and axillary LNs; P = 0.001 for popliteal LN; and P = 0.023 for superficial inguinal LNs). The SWVs for the superficial inguinal and popliteal LNs were significantly lower than those for the mandibular and medial retropharyngeal LNs and higher than those for the axillary LNs (Figure 5).
Box-and-whisker plots for the SWVs for the LNs, including the axillary (A) LN, acquired through SWE in a sagittal scanning plane for the dogs of Figure 4. ‡P < 0.01. See Figure 4 for remainder of key.
Citation: American Journal of Veterinary Research 82, 12; 10.2460/ajvr.82.12.981
Intra- and interobserver intraclass correlation coefficients for each LN are summarized (Table 3). Correlation coefficients were excellent (P < 0.001).
Intra- and interobserver intraclass correlation coefficients (ICCs) for measurement of SWV of the LNs of the dogs of Table 1. Both were excellent (P < 0.001). To evaluate intraobserver reliability, intraday (at least a 6-hour interval between examinations) and interday (at least a 1-week interval between examinations) assessments were performed by 1 investigator. To evaluate interobserver reliability, assessments were performed by 2 other investigators. All investigators were trained in ultrasonography.
| LN | Intraobserver ICC (95% CI) | Interobserver ICC (95% CI) |
|---|---|---|
| Mandibular | 0.863 (0.621–0.960) | 0.933 (0.815–0.981) |
| Medial retropharyngeal | 0.991 (0.975–0.997) | 0.925 (0.793–0.978) |
| Superficial cervical | 0.981 (0.949–0.995) | 0.857 (0.603–0.958) |
| Axillary | 0.921 (0.755–0.974) | 0.873 (0.647–0.963) |
| Superficial inguinal | 0.962 (0.893–0.989) | 0.875 (0.653–0.963) |
| Popliteal | 0.958 (0.882–0.988) | 0.871 (0.643–0.962) |
Discussion
The objectives of the study reported here were to determine the SWVs, through SWE, of various peripheral LNs of healthy dogs; define differences in SWVs among the LNs; evaluate the differences in SWV in relation to the scanning plane and position and size of the ROI; and determine intra- and interobserver agreement for SWVs. Shear-wave velocity for each LN (except the axillary LN) was assessed in each scanning plane at 2 or 3 positions (peripheral, central, or entire) and ROI size (1 X 1 mm for peripheral and central positions and maximum size that did not exceed the size of the LN for measurement of the entire position), owing to their complex intrinsic anatomy. A previous study30 included measurements of shear-wave modulus for the outer and inner cortices and medulla of porcine kidneys. The kidney is a complex, highly compartmentalized, anisotropic organ, with a high level of perfusion. The anisotropy of the renal medulla is predominantly attributable to the perpendicular orientation of the renal tubules to the renal capsule and the convoluted shapes of the distal renal tubules, whereas the renal cortex is not organized in linear structures because the glomeruli have a spherical shape and proximal tubules and distal tubules have a convoluted shape. That study30 revealed that the elastic modulus of the medulla and outer cortex are significantly lower than that of the inner cortex. In the present study, however, significant differences in SWVs based on the cortical and medullary regions of the LNs and the size of ROI were not found in both scanning planes. A possible explanation for this result is that the anatomic intrinsic complexity of LNs is less than that for kidneys. Although an LN is divided into the cortex and medulla, the boundary between these portions is not clear. In another veterinary study,26 the ROI was set as large as possible, avoiding adjacent structures, regardless of specifically examining the LN’s cortex or medulla. For example, when the target organ size was < 2 cm, the ROI was set to fill the target organ by at least 80%. In that study,26 mean ± SD SWVs of the mandibular, medial retropharyngeal, axillary, and superficial inguinal LNs were 1.62 ± 0.07 m/s, 1.57 ± 0.1 m/s, 1.52 ± 0.07 m/s, and 1.55 ± 0.1 m/s, respectively, similar to the SWVs obtained for those LNs in the present study. Therefore, the combined results suggested that the size and location of the ROI did not significantly affect the SWVs for normal LNs, possibly attributable to their small size and typical anatomic location and depth.
The SWVs of the LNs were significantly higher in the sagittal scanning plane than in the transverse scanning plane, similar to the results of other studies30,31 that involved evaluation of skeletal muscles and kidneys. The difference was likely because of tissue anisotropy. In the sagittal scanning plane, SWV was higher when the shear waves were parallel to the orientation of the tissue fibers. Conversely, when the shear waves were perpendicular to the orientation of the tissue fibers in the presence of several interfering tissue interfaces, the speed of the shear waves was lower, and thus SWV was reduced. Although further research is needed to verify LN anisotropy and its effect on SWV, ultrasonographic scanning plane during SWE should be considered when SWV is evaluated.
The axillary LN was located at a depth second to the depth of the deepest LN, the medial retropharyngeal LN, and its SWV was significantly lower than that of the other LNs. The mandibular LN was the most superficial LN, and its SWV was significantly higher, compared with that of the other LNs, except for the medial retropharyngeal LN. One study32 revealed that the depth of an organ has a significant negative correlation with SWV. Although the differences in depths among the LNs in the present study were only a few millimeters, those few millimeter differences may have affected SWVs. However, although the medial retropharyngeal LN was the deepest among the LNs, its SWV was as high as that of the mandibular LN, the most superficial LN, and higher than that of the axillary LN, the second-deepest LN. Shear waves produced by the transducer had to penetrate only adipose tissue for evaluation of the superficial LNs, whereas shear waves had to penetrate the sternocephalicus muscle and mandibular salivary gland in addition to adipose tissue for evaluation of the medial retropharyngeal LN. The results of a previous study33 of people indicated that stretching of the cervical musculature affects the elastic modulus of the cervical LNs. The mean elastic modulus measured in the cervical LNs with static stretch stress of the cervical musculature was significantly higher than that with the neutral condition when shear waves are parallel to the orientation of tissue fibers. Therefore, LN depth and the presence of other tissues between the target tissue and the transducer should be considered when SWV with SWE is evaluated.
Several studies34–36 of people have revealed high intra- and interobserver reliability for SWE assessment of the liver, LNs, spleen, and skeletal muscles. In the present study, intra- and interobserver reliability for the measurement of SWV for all LNs was excellent, indicating limited variability of and operator dependence on data obtained through SWE.
The present study had several limitations. First, dogs varied in age and sex, which may have affected results. However, a study21 of the soft tissues of the neck of people revealed that the elastic modulus of the examined soft tissues is minimally affected by age and sex. Second, histologic examination of the LNs to ensure that they were normal was not performed. To minimize the effect of this limitation, this study was conducted on healthy, relatively young Beagles that had no history of local or systemic diseases, and, following SWE, their LNs (except the medial retropharyngeal LNs) were aspirated, and aspirated cells were examined microscopically. Third, aspiration of the medial retropharyngeal LNs was unsuccessful, so they could not be examined cytologically. Aspiration was unsuccessful because of the LN’s small size and depth relative to the depth of the other LNs, such that the surrounding structures (blood vessels, nerves, or salivary glands) could be damaged with repetitive attempts. Fourth, the LNs from only 1 breed of dog (Beagle) were examined with SWE. Lastly, the SWV of the axillary LN could not be measured from the transverse scanning plane because the ultrasound transducer’s field of view was large (approx 58 mm).
In conclusion, results of the present study indicated that the scanning plane, LN depth, and the presence of interfering tissues between the peripheral LNs and the ultrasound transducer can affect SWVs of those LNs. Intra- and interobserver reliability was excellent. The SWVs obtained for the examined LNs may serve as a reference with which to compare the SWVs obtained for the LNs of other dog breeds and for diseased LNs.
Acknowledgments
The authors thank Canon Medical Systems Korea Co, Ltd. and Roy Park for technical assistance on the ultrasonography and shear wave elastography system.
The authors declare that there were no conflicts of interest.
References
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