Magnetic resonance imaging features of primary lower extremity lymphedema: A retrospective analysis of 228 patients

Mengke Liu; Dingyuan Luo; Xingpeng Li; Yimeng Zhang; Rengui Wang

doi:10.1016/j.jvsv.2024.102004

. 2024 Nov 7;13(2):102004. doi: 10.1016/j.jvsv.2024.102004

Magnetic resonance imaging features of primary lower extremity lymphedema: A retrospective analysis of 228 patients

Mengke Liu ^a,^b, Dingyuan Luo ^c, Xingpeng Li ^a, Yimeng Zhang ^a, Rengui Wang ^a,^∗

PMCID: PMC12014306 PMID: 39515751

Abstract

Background

The value of magnetic resonance imaging (MRI) presentation of primary lower extremity lymphedema in assessing the severity of lower extremity lymphedema is uncertain. The purpose of this study was to assess the role of MRI presentation in staging primary lower extremity lymphedema.

Methods

We enrolled 228 patients with clinically diagnosed primary lower limb lymphoedema from January 2018 to December 2019 in our hospital retrospectively. Patients were divided into stages I, II, and III based on the 2020 International Society of Lymphology clinical staging standards. Two radiologists assessed the following characteristics of the short-term inversion recovery sequence: the extent of edema (longitudinally and transversely); the frequency of MRI manifestations, including the presence of dermal thickening; and the morphology of edema (grid, honeycomb, parallel lines, banded, crescent, and lymphatic lake). The kappa test was used to assess interobserver agreement. The χ² test was used to compare the frequency differences of MRI manifestations between different clinical stages. The Spearman test evaluated the correlation between edema extent and clinical stage.

Results

The extent of edema was correlated positively with clinical stage, both longitudinally and transversely. When comparing stages, the incidence of dermal thickening in stages II and III was significantly higher than in stage I. The incidence of parallel lines in stage I was significantly higher than that in stages II and III. The grid and banded sign incidence in stages I and II were significantly higher than in stage III. The incidence of honeycomb in stages II and III was significantly higher than in stage I. The incidence of lymphatic lake and crescent in stage III was significantly higher than in stages I and II (P < .001).

Conclusions

Short-term inversion recovery can sensitively diagnose lymphedema and assist in clinical staging. MRI manifestations of primary lower extremity lymphedema in different stages have specific MRI features.

Keywords: Primary lymphedema, Lower extremity, MRI, Staging

Article Highlights.

•
Type of Research: Single-center retrospective cohort study
•
Key Findings: When comparing stages, the incidence of dermal thickening in stages II and III was significantly higher than in stage I; the incidence of parallel lines in stage I was significantly higher than that in stages II and III; the grid and banded sign incidence in stages I and II was significantly higher than in stage III; the incidence of honeycomb in stages II and III was significantly higher than in stage I; and the incidence of lymphatic lake and crescent in stage III was significantly higher than in stages I and II (P < .001).
•
Take Home Message: Primary lower extremity lymphedema has diverse magnetic resonance imaging features and characteristic magnetic resonance imaging presentations in patients with different clinical disease stages. This study provides a specific basis for the clinical staging of primary lower extremity lymphedema.

Lower extremity lymphedema is a chronic disease characterized by soft tissue swelling and skin fibrosis, caused by the accumulation of protein-rich fluid in the interstitium, leading to disproportionate lymphatic production and entry into the circulatory system and abnormal proliferation of fibroblasts and adipocytes.¹ Primary lower extremity lymphedema is caused by genetic mutations that result in lymphatic hypoplasia and lymphatic drainage restriction.² Secondary lower extremity lymphedema results from damage or obstruction to the lymphatic system and is commonly seen after gynecological malignancy surgery.³ Patients with primary lower extremity lymphedema initially present with painless swelling of one limb, often starting at the dorsum of the foot, gradually involving the calf and even the thigh, with disease progression, leading to limb heaviness, discomfort, and mobility impairment. Based on the clinical presentation of patients, the International Society of Lymphology (ISL) divides lower extremity lymphedema into four stages.⁴ Stage 0 is a subclinical symptom; stage I is characterized by fluid accumulation in the interstitium; stage II involves subcutaneous soft tissue adipose deposition and fibrosis. Stage III often involves skin changes, such as pigmentation and verrucous hyperplasia, which can progress to elephantiasis.

Previously, the imaging diagnosis of lower extremity lymphedema relied heavily on lymphoscintigraphy, which can identify lymphatic reflux disorders, including asymmetric and delayed imaging of inguinal lymph nodes, the formation of collateral lymphatic vessels, and the presence of dermal backflow.⁵^,⁶ However, lymphoscintigraphy has low spatial resolution and a poor display of delicate anatomical structures, making it difficult to assess the severity of limb swelling in lymphedema patients. Magnetic resonance imaging (MRI) is noninvasive, radiation free, and has a much higher soft tissue resolution than lymphoscintigraphy, which can show clearly the various layers of limb anatomy and distinguish the distribution of lymph and fat in the subcutaneous soft tissue, reflecting the progression and changes of primary lymphedema, and is used increasingly for the diagnosis and severity evaluation of primary lower extremity lymphedema.⁵^,7, 8, 9, 10

In previous studies, the morphological diversity of lymphatic fluid in the subcutaneous soft tissue of patients with secondary upper extremity lymphedema caused by breast cancer has been observed using MRI.¹¹ This study aims to establish the relationship between MRI findings and clinical staging of primary lower extremity lymphedema by exploring the differences in imaging manifestations among patients with different clinical stages of primary lower extremity lymphedema.

Methods

Patients

This retrospective study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and was approved by the ethics committee of our hospital. Informed consent was waived because the study was a retrospective review. The study retrospectively reviewed patients who visited the lymphatic surgery department of our hospital between January 2018 and December 2019 for primary lower extremity lymphedema, according to the following inclusion criteria: (1) diagnosed lower extremity lymphedema by lymphoscintigraphy, (2) edema with no apparent incentive, and (3) underwent the lower extremities MRI. Exclusion criteria included: (1) incomplete clinical data, making it difficult to determine the clinical stage accurately, (2) poor MRI quality, and (3) lower extremity lymphedema caused by secondary factors such as postoperative malignant tumors, trauma, filariasis, and infection (Fig 1).

Fig 1 — Flowchart of participants. *MRI*, magnetic resonance imaging.

Using the 2020 clinical staging criteria of the ISL as a reference,⁴ experienced lymphatic surgeons at our institution categorized patients into stages I, II, and III; there were no patients with stage 0 disease in this study. Patients underwent no formal clinical interventions before MRI, and there were no adverse events during the entire study.

MRI examination

All MRI examinations were performed using a 1.5 T scanner (Intera Ingenia, Phillips, Best, the Netherlands) with a 16-channel body surface coil. The sequences of lower extremity MRI include short-term inversion recovery (STIR) and mDIXON sequences in coronal and axial planes. The STIR parameters were as follows: TR, 8549 ms; TE, 165 ms; field of view, 400 mm × 400 mm; and slice thickness, 7 mm. The mDixon parameters were as follows: TR, 5.87 ms; TE1, 1.8 ms; TE2, 4.0 ms; slice thickness, 8 mm; voxel, 1.5 mm²; and field of view, 420 mm × 420 mm. Patients were scanned in a supine position, and three sets of images were acquired consecutively at three different stations: the thigh (first station), calf (second station), and ankle (third station).

Image analysis

Two senior radiologists analyzed MR characterization using coronal and transverse axial STIR sequences without knowing the clinical staging of the patient. The area of interest was the most severe region of edema, and the analysis included the following.

(1)
The extent of edema involvement, evaluated in terms of longitudinal range (accumulation on one side of the knee joint and less than one-half of the limb or more than one-half of the limb) and transverse range (horizontal infiltration at <50%, 50%-75%, or 75%-100% of the circumference).
(2)
Evaluation of skin thickening in the area of interest, defined as dermal thickness of >2 mm.⁹
(3)
Observation of edema infiltration morphology in the subcutaneous soft tissues and fascial areas of interest, using several signs such as the parallel line sign, grid sign, honeycomb sign, band sign, lymphatic lake, and crescent sign (Fig 2, Fig 3, Fig 4). Each sign was defined as follows:
- •
  The parallel lines were thin, 1 to 2 mm wide, and parallel to the superficial fascia, not forming a network.
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  The grid signs were multiple intertwined lines, ≤3 mm wide, with the largest meridian parallel to the superficial fascia and a width-to-length ratio of less than 2:3.
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  The honeycomb signs represented a further thickening of the grid in more than two directions, with a wall thickness of >3 mm and a width-to-length ratio of greater than 2:3.
- •
  The band sign is an accumulation of fluid on the fascial surface with a strip-like structure observed at the axial level.
- •
  The crescent sign is a subfascial accumulation observed at the axial level.
- •
  The lymphatic lake is a large, structureless area of edema located in the subcutaneous soft tissue.

Fig 2 — A 25-year-old man with bilateral lower limb lymphoedema, International Society of Lymphology (ISL) stage I. Short-term inversion recovery (STIR) demonstrates the slight swelling of the affected limb. Coronal view **(A)** shows the uppermost edge of the edema is located below the knee, parallel line sign (arrow) is seen in the axial view **(B)**, with no dermal thickening on the affected side.

Fig 3 — A 20-year-old man with bilateral lower limb lymphoedema, International Society of Lymphology (ISL) stage II. Short-term inversion recovery (STIR) demonstrates the moderate swelling of the affected limb. Coronal view **(A)** shows the edema involving the entire lower extremity, up to the root of the thigh, grid sign (thin arrow) and banded sign (thick arrow) is seen in the axial view **(B)**; dermal thickening is seen on the affected side.

Fig 4 — (A and B) A 37-year-old woman with bilateral lower limb lymphoedema, International Society of Lymphology (ISL) stage III. Short-term inversion recovery (STIR) demonstrates the severe swelling of the affected limb. Coronal view **(A)** shows the edema involving the entire lower extremity, up to the hip, and lymphatic lake sign (asterisk) is seen in the axial view **(B)**, dermal thickening is seen on the affected side. **(C)** A 38-year-old man with bilateral lower limb lymphoedema, ISL stage III, honeycomb sign (thin arrow) and crescent sign (thick arrow) is seen in the axial position.

A positive sign was recorded as 1, and a negative sign was recorded as 0. The frequency of MRI manifestations was recorded and compared between and within different clinical stages.

Statistical analysis

Data analysis was performed using SPSS 23.0 (SPSS, Inc., Chicago, IL). The Spearman test was used to analyze the correlation between longitudinal and cross-sectional extent and clinical staging. Differences in the frequency of MRI manifestations under different clinical stages of lower extremity lymphedema were evaluated using the χ² or Fisher's exact test. Multiple comparisons were performed using the χ² test with correction for P values, and differences were considered significant at a P value of <.0167.

Results

Patients population

A total of 349 patients with primary lower extremity lymphedema were collected, and 228 patients were included after inclusion and exclusion criteria, including 144 female (63%) and 84 male (37%) participants ranging in age from 2 to 76 years (mean age, 32.86 years). The duration of edema ranged from 0 to 50 years, with an average duration of 11.63 years. Of the participants, 216 (94.7%) had an initial onset of edema in their calves, and 12 (6.3%) had an onset in their thighs.

One hundred thirty participants (57%) had unilateral lower extremity lymphedema, and 98 (43%) had bilateral lower extremity lymphedema. In patients with bilateral lower extremity lymphedema, the onset of edema was bilateral in 56 of 98 cases (57.1%). In comparison, it started on the right lower extremities in 27 of 98 (27.6%) and on the left in 15 of 98 (15.3%) cases. The swelling was symmetrical in 40 of 98 cases (40.8%) and asymmetrical in 58 of 98 cases (59.2%). Of the cases with bilateral lower extremity lymphedema, 20 (8.8%) were diagnosed initially as unilateral based on lymphoscintigraphy, but MRI revealed high signal intensity in the subcutaneous soft tissues bilaterally, indicating bilateral lower extremity lymphedema.

The patients were classified into clinical stages I, II, and III, with 96 (42%), 79 (34%), and 53 (23%) patients in each stage, respectively (as shown in Fig 2, Fig 3, Fig 4). The detailed clinical data can be found in Table I.

Table I.

Clinical characteristics of patients

	I (n = 96）	II (n = 79）	III (n = 53)
Age, years	27.46 ± 15.54	38.49 ± 17.22	34.25 ± 17.07
Onset age, years	21.32 ± 15.92	25.10 ± 17.76	15.77 ± 16.80
Course, years	6.24 ± 8.34	13.45 ± 12.35	18.67 ± 12.03
Sex
Female	71 (74.0)	47 (59.5)	26(49.1)
Male	25 (26.0)	32 (40.5)	27(50.9)

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Values are mean ± standard deviation or number (%).

Interrater consistency comparison

Interrater agreement was good in the assessment of the parallel line sign (kappa = 0.970), grid sign (kappa = 0.973), honeycomb sign (kappa = 0.962), stripe sign (kappa = 0.957), lymph lake (kappa = 0.960), and crescent sign (kappa = 0.934), and dermal thickening (kappa = 0.936).

Relationship between lower extremity lymphedema clinical stage and longitudinal extent

The longitudinal extent of edema showed a positive correlation with the clinical stage (r = 0.580). Among the 228 patients, 93 (40.8%) had edema that extended below the knee, and 135 (59.2%) had edema that affected the entire lower limb. The incidence of edema affecting the entire lower limb in stages II and III was significantly higher than in stage I (P < .001).

Relationship between lower extremity lymphedema clinical stage and transverse extent of edema

The transverse extent of edema also showed a positive correlation with the clinical stage (R = 0.428). Among the 228 patients, 175 (76.8%) had edema that affected 75% to 100% of the circumference, 44 (19.3%) had edema that affected 50% to 75% of the circumference, and 9 (3.9%) had edema that affected <50% of the circumference (Table II, Fig 5). Stages II and III have a greater incidence of edema infiltration between 75% and 100% of the circumference than stage I and a smaller incidence of infiltration below 75% of the circumference than stage I.

Table II.

Presence of magnetic resonance (MR) characteristics and corresponding number of cases and rate, with correlation with lower extremity lymphedema stage

	I (n = 96）	II (n = 79）	III (n = 53)	P value
	I (n = 96）	II (n = 79）	III (n = 53)	I vs II	II vs III	I Vs III
Dermal thickening	21 (21.8)	65 (82.2)	52 (98.1)	<.001^a	.018	<.001^a
Subcutaneous lymphoedema pattern
Grid	65 (67.7)	56 (70.8)	14 (26.4)	.651	<.001^a	<.001^a
Honeycomb	2 (2.0)	46 (58.2)	35 (66.0)	<.001^a	.366	<.001^a
Parallel line	64 (66.7)	10 (12.6)	0 (0)	<.001^a	.018	<.001^a
Banded	79 (82.2)	66 (83.5)	20 (37.7)	.827	<.001^a	<.001^a
Lymphatic lake	0 (0)	2 (2.5)	27 (50.9)	.202	<.001^a	<.001^a
Crescent	0 (0)	4 (5.0)	22 (41.5)	.040	<.001^a	<.001^a
Range of lengthways				<.001^a	.001	<.001^a
The whole lower limb	26 (27.1)	58 (73.4)	51 (96.1)
Above or below the knee	70(72.9)	21 (26.5)	2 (3.9)
Range of horizontal				<.001^a	.684	<.001^a
75%-100%	52 (55.2)	72 (91.1)	51 (96.1)
50%-75%	36 (37.5)	6 (7.6)	2 (3.9)
<50%	8 (7.3)	1 (1.3)	0 (0)

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P < .0167.

Fig 5 — **(A-H)** Graphs showing different magnetic resonance (MR) characteristics of primary lower limb lymphoedema and their distribution (patients' number in ordinate) according to the lower extremity lymphedema clinical staging (in the abscissa).

Relationship between lower extremity lymphedema clinical stage and soft tissue, subcutaneous tissue, fascia area, edema infiltration form, and skin thickening

There was a significant difference in the incidence of parallel line sign, grid sign, honeycomb sign, stripe sign, lymph lake, and crescent sign among the three groups (P < .001). The incidence of parallel line sign in stage I was significantly higher than in stages II and III, the incidence of grid sign in stages I and II was significantly higher than in stage III, the incidence of honeycomb sign in stages II and III were higher than in stage I, and the incidence of stripe sign in stages I and II was higher than in stage III. The incidence of lymph lake and crescent sign in stage III was higher than in stages I and II (P < .001).

There was also a statistical difference in the incidence of skin thickening among the three groups (P < .001). When comparing the three groups, the incidence of skin thickening in stages II and III was significantly higher than in stage I (P < .001) (Table II, Fig 5).

Discussion

Our study shows that primary lower extremity lymphedema has diverse MRI features and characteristic MRI presentations in patients with different clinical stages. This work provides a specific basis for the clinical staging of primary lower extremity lymphedema. In addition, MRI can detect lower extremity lymphedema with normal lymphatic vessels on scintigraphy, providing high sensitivity for diagnosing subclinical lower extremity lymphedema.

Primary lower extremity lymphedema is a rare congenital or developmental anomaly of the lymphatics.⁴^,¹²^,¹³ The calf anterior lymphatic vessels are the weak link in the lower limb lymphatic pathway and the site where lymphedema occurs earliest and most severely.¹⁴ In this study, most patients initially had localized symptoms in the lower leg or ankle, which gradually progressed to the thigh with disease progression and eventually affected the entire lower limb, consistent with previous literature reports. However, in this study, 5% of patients had initial symptoms in the thigh, which gradually progressed downward and affected the lower leg. This pattern may be related to the development direction of primary lower extremity lymphedema, which has two directions: upward and downward. The former is due to pathological changes in the wall and lymph nodes of the lymphatic vessels, such as poor development, closure, interruption, or increased number, expansion, and deformation, resulting in lymphatic reflux obstruction, capillary lymphatic expansion, increased intraluminal pressure, and increased initial segment flow rate, leading to the opening of a large number of small-diameter bypass lymphatic vessels and increased pressure wave amplitude.¹⁵ The latter is due to increased lymphatic system pressure caused by chyle reflux obstruction, with lymph fluid refluxing from the thoracic duct and chyle pool to the lower extremities, leading to limb swelling.¹⁶ The former is due to mechanical incompetence or valve defects or dysfunction, whereas the latter is caused by chyle reflux, which has a more complex mechanism than the former.

In this study, 8.8% of patients with lower extremity lymphedema exhibited no apparent swelling, had negative clinical symptoms, and had clear lymphatic vessel visualization on lymphoscintigraphy with unobstructed imaging agent reflux. However, a high signal intensity was observed in the subcutaneous fat layer on STIR sequences, indicating that STIR is more sensitive for detecting lower extremity lymphedema in patients with no apparent positive symptoms and normal lymphatic vessel reflux. STIR is a special fat suppression sequence that can eliminate the high signal of adipose tissue on T2-weighted imaging and enhance the signal of water, thus intuitively and sensitively displaying high-signal edema, which is of great significance for early detection of subclinical edema in limb lesions.¹⁷

MRI examination has high soft tissue resolution, can display the various layers of limb anatomy, accurately determines the location of edema, and, to a certain extent, reflects the progression of primary lymphedema.¹⁸ It can identify the extent of lymphedema within the limb. This study used the coronal and transverse planes to observe the spatial extent of edema. It was found that, in >50% of patients with stage I disease, edema was confined to above or below the knee joint, whereas in >95% of patients with stage III disease, edema involved the entire lower limb (both above and below the knee joint). By observing the axial distribution of edema, it was found that, in >90% of patients with stage II and III disease, fluid permeation at any level may exceed 75%. In contrast, in stage I, only 55% of patients had fluid permeation exceeding 75%, which was significantly lower than the other two stages. The spatial distribution of lower limb fluid permeation reflects the progression of the disease, and observing it can provide auxiliary assistance for clinical staging.

In the present study, we observed significant correlations between the different morphologies of edematous infiltrates within the subcutaneous soft tissues, in the fascial areas, and between dermal thickening and clinical staging. Different MRI features had suggestive roles in clinical staging: in stage I patients, the parallel line sign, grid sign, and band sign were predominant; in stage II patients, the grid sign, honeycomb sign, and band sign were predominant; and in stage III patients, crescent signs and lymphatic lakes were the main manifestations. We believe that these phenomena are related closely to the progression of lymphedema. In the early stage of lymphedema, the lymphatic fluid in the interstitial space increases owing to poor lymphatic drainage, and the dilated lymphatic vessels and exudate can appear as parallel lines or mesh patterns on MRI. Meanwhile, the lymphatic leakage fluid is located on the fascia as a band-like high signal. In this study, the parallel line sign, grid sign, and band sign were predominant in stage I patients, with the highest incidence of parallel line sign, which was significantly higher than in stage II and III patients. However, there was no significant difference between stage I and II in the occurrence of grid sign and band sign (P > .05). Therefore, the parallel line sign can be used as a characteristic sign of lower extremity lymphedema stage I. As the disease progresses, fibrous tissue and lymphatic fluid accumulate around the subcutaneous adipose tissue. Thick deposits of collagen fibers can be observed, forming a typical honeycomb pattern.¹⁴ There was a significant difference in the presence of honeycomb patterns between stage I and II or III, but no significant difference between stages II and III. Therefore, honeycomb patterns highly suggest that patients have entered stage II. In the middle and late stages of the disease, the lymphatic fluid accumulated in the subcutaneous fat gradually spreads to the fascial surface and subfascial under the pressure gradient. The dense fascia structure impedes the diffusion of lymphatic fluid, causing it to stagnate and exacerbate the obstruction of lymphatic reflux. As a result, the limb continues to thicken, and a lymphatic lake-like appearance can be observed on MRI. In the late stage of edema, when the lymphatic fluid breaks through the fascia and reaches below it, a crescent-shaped high signal can be seen on MRI, defined as the crescent sign. In this study, the incidence of crescent signs and lymphatic lakes in stage III patients was significantly higher than in stage II and I patients, and there was no significant difference between stages I and II. This finding indicates that the crescent sign and lymphatic lake can be used as characteristic signs of stage III lymphedema.

This study found that the incidence of skin thickening in stage I lymphedema was significantly lower than in stages II and III. Skin thickening mainly occurred in stages II and III, but there was no significant difference in skin thickening between adjacent groups. This finding suggests that skin thickening is a sign of lower extremity lymphedema disease progression and can be helpful for the clinical staging of lower extremity lymphedema. Skin thickening is a pathological result of skin fibrosis. Electron microscopy observations of the limb tissue of secondary lower limb lymphedema patients show progressive collagen fiber deposition in the dermal tissue, indicating that lymphatic vessel damage can lead to dermal tissue inflammation, progressive fibrosis, and remodeling, which are signs of late-stage lymphedema.¹⁹ In Cellina et al's study,¹⁴ dermal thickening was significantly positively correlated with clinical staging, which supports the results of our study.

This study has several limitations. First, this study only analyzed STIR sequence images and did not compare them with other MRI sequences. Second, the patients in this study were all selected from primary lower extremity lymphedema cases, and secondary patients were not included for comparative analysis. Third, this study does not count additional factors, such as the morphology of the distal lymphatic vessels and the number of draining lymph nodes. Finally, this study only addressed the correlation between the lymphedema stage and its imaging signs and did not address age heterogeneity.

In summary, the MRI manifestations of lymphedema provide some diagnostic basis for the clinical staging of lower extremity lymphedema, with the parallel line sign as a characteristic sign of stage I, the honeycomb sign as a characteristic sign of stage II, and the crescent and lymphatic lake signs as characteristic signs of stage III. MRI can be used as a noninvasive imaging technique diagnosing and evaluating primary lower extremity lymphedema, and it has an auxiliary diagnostic role in clinical staging.

Author Contributions

Conception and design: ML, DL, ZY, RW

Analysis and interpretation: ML, DL, XL, RW

Data collection: ML, DL, XL, ZY

Writing the article: ML, ZY, RW

Critical revision of the article: ML, DL, XL, ZY, RW

Final approval of the article: ML, DL, XL, ZY, RW

Statistical analysis: ML, ZY

Obtained funding: ML, RW

Overall responsibility: RW

Funding

This study was supported by the National Natural Science Foundation of China (No. 61876216).

Disclosures

None.

Footnotes

The editors and reviewers of this article have no relevant financial relationships to disclose per the Journal policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest.

References

1.Maclellan R.A., Greene A.K. Lymphedema. Semin Pediatr Surg. 2014;23:191–197. doi: 10.1053/j.sempedsurg.2014.07.004. [DOI] [PubMed] [Google Scholar]
2.Li C.Y., Kataru R.P., Mehrara B.J. Histopathologic features of lymphedema: a molecular review. Int J Mol Sci. 2020;21:2546. doi: 10.3390/ijms21072546. [DOI] [PMC free article] [PubMed] [Google Scholar]
3.Leung E.Y., Tirlapur S.A., Meads C. The management of secondary lower limb lymphoedema in cancer patients: a systematic review. Palliat Med. 2015;29:112–119. doi: 10.1177/0269216314545803. [DOI] [PubMed] [Google Scholar]
4.Executive Committee of the International Society of Lymphology The diagnosis and treatment of peripheral lymphedema: 2020 consensus document of the International Society of Lymphology. Lymphology. 2020;53:3–19. [PubMed] [Google Scholar]
5.Pappalardo M., Cheng M.H. Lymphoscintigraphy for the diagnosis of extremity lymphedema: current controversies regarding protocol, interpretation, and clinical application. J Surg Oncol. 2020;121:37–47. doi: 10.1002/jso.25526. [DOI] [PubMed] [Google Scholar]
6.Lam M.C., Luk W.H., Tse K.H. Lymphoscintigraphy in the evaluation of lower extremity lymphedema: local experience. Hong Kong Med J. 2014;20:121–125. doi: 10.12809/hkmj133988. [DOI] [PubMed] [Google Scholar]
7.Lu Q., Xu J., Liu N. Chronic lower extremity lymphedema: a comparative study of high-resolution interstitial MR lymphangiography and heavily T2-weighted MRI. Eur J Radiol. 2010;73:365–373. doi: 10.1016/j.ejrad.2008.10.041. [DOI] [PubMed] [Google Scholar]
8.Du X., Liu C. Application of imaging in lymphedema surgical therapies. Gland Surg. 2020;9:582–588. doi: 10.21037/gs.2020.03.24. [DOI] [PMC free article] [PubMed] [Google Scholar]
9.Arrivé L., Derhy S., Dahan B., et al. Primary lower limb lymphoedema: classification with non-contrast MR lymphography. Eur Radiol. 2018;28:291–300. doi: 10.1007/s00330-017-4948-z. [DOI] [PubMed] [Google Scholar]
10.Cellina M., Oliva G., Menozzi A., Soresina M., Martinenghi C., Gibelli D. Non-contrast magnetic resonance lymphangiography: an emerging technique for the study of lymphedema. Clin Imaging. 2019;53:126–133. doi: 10.1016/j.clinimag.2018.10.006. [DOI] [PubMed] [Google Scholar]
11.Kim G., Donohoe K., Smith M.P., et al. Use of non-contrast MR in diagnosing secondary lymphedema of the upper extremities. Clin Imaging. 2021;80:400–405. doi: 10.1016/j.clinimag.2021.08.018. [DOI] [PubMed] [Google Scholar]
12.Senger J.B., Kadle R.L., Skoracki R.J. Current concepts in the management of primary lymphedema. Medicina (Kaunas) 2023;59:894. doi: 10.3390/medicina59050894. [DOI] [PMC free article] [PubMed] [Google Scholar]
13.Grada A.A., Phillips T.J. Lymphedema: pathophysiology and clinical manifestations. J Am Acad Dermatol. 2017;77:1009–1020. doi: 10.1016/j.jaad.2017.03.022. [DOI] [PubMed] [Google Scholar]
14.Liu N.F., Yan Z.X., Wu X.F., Luo Y. Magnetic resonance lymphography demonstrates spontaneous lymphatic disruption and regeneration in obstructive lymphedema. Lymphology. 2013;46:56–63. [PubMed] [Google Scholar]
15.Duhon B.H., Phan T.T., Taylor S.L., Crescenzi R.L., Rutkowski J.M. Current mechanistic understandings of lymphedema and lipedema: tales of fluid, fat, and fibrosis. Int J Mol Sci. 2022;23:6621. doi: 10.3390/ijms23126621. [DOI] [PMC free article] [PubMed] [Google Scholar]
16.Kazemzadeh G.H., Sadeghi R., Ebrahimi E., Rad M.A. Lower limb lymphoscintigraphy in diagnosis of chylous reflux lymphedema. Chin J Med Imaging Technol. 2016;32:1731–1734. [Google Scholar]
17.Cellina M., Martinenghi C., Panzeri M., et al. Noncontrast MR lymphography in secondary lower limb lymphedema. J Magn Reson Imaging. 2021;53:458–466. doi: 10.1002/jmri.27328. [DOI] [PubMed] [Google Scholar]
18.Kim G., Smith M.P., Donohoe K.J., Johnson A.R., Singhal D., Tsai L.L. MRI staging of upper extremity secondary lymphedema: correlation with clinical measurements. Eur Radiol. 2020;30:4686–4694. doi: 10.1007/s00330-020-06790-0. [DOI] [PubMed] [Google Scholar]
19.Tashiro K., Feng J., Wu S.H., et al. Pathological changes of adipose tissue in secondary lymphoedema. Br J Dermatol. 2017;177:158–167. doi: 10.1111/bjd.15238. [DOI] [PubMed] [Google Scholar]

[bib1] 1.Maclellan R.A., Greene A.K. Lymphedema. Semin Pediatr Surg. 2014;23:191–197. doi: 10.1053/j.sempedsurg.2014.07.004. [DOI] [PubMed] [Google Scholar]

[bib2] 2.Li C.Y., Kataru R.P., Mehrara B.J. Histopathologic features of lymphedema: a molecular review. Int J Mol Sci. 2020;21:2546. doi: 10.3390/ijms21072546. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib3] 3.Leung E.Y., Tirlapur S.A., Meads C. The management of secondary lower limb lymphoedema in cancer patients: a systematic review. Palliat Med. 2015;29:112–119. doi: 10.1177/0269216314545803. [DOI] [PubMed] [Google Scholar]

[bib4] 4.Executive Committee of the International Society of Lymphology The diagnosis and treatment of peripheral lymphedema: 2020 consensus document of the International Society of Lymphology. Lymphology. 2020;53:3–19. [PubMed] [Google Scholar]

[bib5] 5.Pappalardo M., Cheng M.H. Lymphoscintigraphy for the diagnosis of extremity lymphedema: current controversies regarding protocol, interpretation, and clinical application. J Surg Oncol. 2020;121:37–47. doi: 10.1002/jso.25526. [DOI] [PubMed] [Google Scholar]

[bib6] 6.Lam M.C., Luk W.H., Tse K.H. Lymphoscintigraphy in the evaluation of lower extremity lymphedema: local experience. Hong Kong Med J. 2014;20:121–125. doi: 10.12809/hkmj133988. [DOI] [PubMed] [Google Scholar]

[bib7] 7.Lu Q., Xu J., Liu N. Chronic lower extremity lymphedema: a comparative study of high-resolution interstitial MR lymphangiography and heavily T2-weighted MRI. Eur J Radiol. 2010;73:365–373. doi: 10.1016/j.ejrad.2008.10.041. [DOI] [PubMed] [Google Scholar]

[bib8] 8.Du X., Liu C. Application of imaging in lymphedema surgical therapies. Gland Surg. 2020;9:582–588. doi: 10.21037/gs.2020.03.24. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib9] 9.Arrivé L., Derhy S., Dahan B., et al. Primary lower limb lymphoedema: classification with non-contrast MR lymphography. Eur Radiol. 2018;28:291–300. doi: 10.1007/s00330-017-4948-z. [DOI] [PubMed] [Google Scholar]

[bib10] 10.Cellina M., Oliva G., Menozzi A., Soresina M., Martinenghi C., Gibelli D. Non-contrast magnetic resonance lymphangiography: an emerging technique for the study of lymphedema. Clin Imaging. 2019;53:126–133. doi: 10.1016/j.clinimag.2018.10.006. [DOI] [PubMed] [Google Scholar]

[bib11] 11.Kim G., Donohoe K., Smith M.P., et al. Use of non-contrast MR in diagnosing secondary lymphedema of the upper extremities. Clin Imaging. 2021;80:400–405. doi: 10.1016/j.clinimag.2021.08.018. [DOI] [PubMed] [Google Scholar]

[bib12] 12.Senger J.B., Kadle R.L., Skoracki R.J. Current concepts in the management of primary lymphedema. Medicina (Kaunas) 2023;59:894. doi: 10.3390/medicina59050894. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib13] 13.Grada A.A., Phillips T.J. Lymphedema: pathophysiology and clinical manifestations. J Am Acad Dermatol. 2017;77:1009–1020. doi: 10.1016/j.jaad.2017.03.022. [DOI] [PubMed] [Google Scholar]

[bib14] 14.Liu N.F., Yan Z.X., Wu X.F., Luo Y. Magnetic resonance lymphography demonstrates spontaneous lymphatic disruption and regeneration in obstructive lymphedema. Lymphology. 2013;46:56–63. [PubMed] [Google Scholar]

[bib15] 15.Duhon B.H., Phan T.T., Taylor S.L., Crescenzi R.L., Rutkowski J.M. Current mechanistic understandings of lymphedema and lipedema: tales of fluid, fat, and fibrosis. Int J Mol Sci. 2022;23:6621. doi: 10.3390/ijms23126621. [DOI] [PMC free article] [PubMed] [Google Scholar]

[bib16] 16.Kazemzadeh G.H., Sadeghi R., Ebrahimi E., Rad M.A. Lower limb lymphoscintigraphy in diagnosis of chylous reflux lymphedema. Chin J Med Imaging Technol. 2016;32:1731–1734. [Google Scholar]

[bib17] 17.Cellina M., Martinenghi C., Panzeri M., et al. Noncontrast MR lymphography in secondary lower limb lymphedema. J Magn Reson Imaging. 2021;53:458–466. doi: 10.1002/jmri.27328. [DOI] [PubMed] [Google Scholar]

[bib18] 18.Kim G., Smith M.P., Donohoe K.J., Johnson A.R., Singhal D., Tsai L.L. MRI staging of upper extremity secondary lymphedema: correlation with clinical measurements. Eur Radiol. 2020;30:4686–4694. doi: 10.1007/s00330-020-06790-0. [DOI] [PubMed] [Google Scholar]

[bib19] 19.Tashiro K., Feng J., Wu S.H., et al. Pathological changes of adipose tissue in secondary lymphoedema. Br J Dermatol. 2017;177:158–167. doi: 10.1111/bjd.15238. [DOI] [PubMed] [Google Scholar]

PERMALINK

Magnetic resonance imaging features of primary lower extremity lymphedema: A retrospective analysis of 228 patients

Mengke Liu, MD

Dingyuan Luo, MMed

Xingpeng Li, MMed

Yimeng Zhang, MMed

Rengui Wang, MD

Abstract

Background

Methods

Results

Conclusions

Article Highlights.

Methods

Patients

Fig 1.

MRI examination

Image analysis

Fig 2.

Fig 3.

Fig 4.

Statistical analysis

Results

Patients population

Table I.

Interrater consistency comparison

Relationship between lower extremity lymphedema clinical stage and longitudinal extent

Relationship between lower extremity lymphedema clinical stage and transverse extent of edema

Table II.

Fig 5.

Relationship between lower extremity lymphedema clinical stage and soft tissue, subcutaneous tissue, fascia area, edema infiltration form, and skin thickening

Discussion

Author Contributions

Funding

Disclosures

Footnotes

References

ACTIONS

PERMALINK

RESOURCES

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