Fluid Distribution Patterns in Early Stage Upper Extremity Lymphedema

Abstract

Introduction

MRI Stage 1 (early stage) upper extremity lymphedema is characterized by fluid infiltration in the subcutaneous tissues that do not exceed 50% of the extremity circumference at any level. The spatial fluid distribution in these cases has not been detailed and may be important to help determine the presence and location of compensatory lymphatic channels. The aim of this study was to determine if there was a pattern of distribution of fluid infiltration in patients with early-stage lymphedema that could correspond to known lymphatic pathways in the upper extremity.

Methods

A retrospective review identified all patients with MRI stage 1 upper extremity lymphedema who were evaluated at a single lymphatic center. Using a standardized scoring system, a radiologist graded the severity of fluid infiltration at 18 anatomical locations. A cumulative spatial histogram was then created to map out regions where fluid accumulation occurred most and least frequently.

Results

Eleven patients with MRI stage 1 upper extremity lymphedema were identified between January 2017 and January 2022. The mean age was 58 years and the mean BMI was 30 m/kg². One patient had primary lymphedema and the remaining ten had secondary lymphedema. The forearm was affected in nine cases, and fluid infiltration was predominantly concentrated along the ulnar aspect, followed by the volar aspect, while the radial aspect was completely spared. Within the upper arm, fluid was primarily concentrated distally and posteriorly, and occasionally medially.

Conclusion

In patients with early-stage lymphedema, fluid infiltration is concentrated along the ulnar forearm and the posterior distal upper arm, which aligns with the tricipital lymphatic pathway. There is also sparing of fluid accumulation along the radial forearm in these patients, suggesting a more robust lymphatic drainage along this region, possibly due to a connection to the lateral upper arm pathway.

INTRODUCTION

Upper extremity lymphedema results from insufficiency of the lymphatic system. Patients present with swelling and decreased mobility which can severely diminish quality of life. Untreated lymphedema is typically progressive and can lead to increased edema and fat hypertrophy and continued limb enlargement. Despite the expected course of disease progression, there is considerable variation in the severity of disease at the time of initial presentation with some patients presenting with relatively mild manifestations or even in a subclinical stage of limb swelling.^1–3 There are multiple ways to evaluate or grade upper extremity lymphedema including bioimpedance, circumferential measurements, and perometry. As MRI is able to differentiate soft tissues, lymphedema can more be objectively graded using an MRI grading system to determine the extent of the fluid component within the extremity.^4,5 While the severity of edema can be defined using this grading system, spatial patterns of fluid distribution along the affected extremity in those with primary and secondary upper extremity lymphedema have not been well studied.

During the validation of an MRI grading system, one group previously noticed a general pattern of fluid infiltration along the elbow and the posterior aspect of the upper arm.⁴ In another study, the authors examined edema distribution patterns in patients with breast cancer related lymphedema and noted that areas spared from edema were centered around the cephalic vein in the upper arm.⁶ However, a study on patients with lower extremity lymphedema but did not observe any consistent patterns in fluid distribution in lymphedematous extremities.⁷ There have been no prior studies focusing on edema distribution patterns, particularly at early stages before these patterns become indistinguishable due to more diffuse edema.

Knowledge of the spatial patterns of edema in lymphedema may reveal areas of lymphatic vulnerability. Furthermore, disease-free areas may reflect zones of compensated or more robust drainage.⁶ The purpose of this study was to determine these patterns of edema in the upper extremities of patients with early-stage lymphedema.

METHODS

A retrospective review of our MRL lymphatic center database was performed. Institutional review board approval was obtained (Protocol # 2018P000085). Consecutive patients with MRI stage 1 upper extremity lymphedema were identified using a previously-validated MRI staging system.⁴ Briefly, MRI stage upper extremity lymphedema was defined by fluid infiltration in the subcutaneous tissue that did not exceed 50% of the circumference of the forearm or upper arm at any level.⁴

Patient demographics were extracted from the lymphatic center database and MRI reports were reviewed to identify all patients with MRI Stage 1 upper extremity lymphedema. Using a standardized scoring system, an attending radiologist with fellowship training in MRI (L.L.T.) graded the severity of fluid infiltration at 5 levels along the hand, forearm, and upper arm, across a total of 18 anatomical locations (Figure 1). Grades of 0–3 were assigned based on the severity of edema in that region with grade 0 being no edema, grade 1 being less than 25% fluid by volume across the subcutaneous fat or with dermal thickening only, grade 2 between 25–50% fluid by volume and 3 indicating greater than 50% fluid by volume. Data were analyzed in Microsoft Excel (Microsoft 2021, Redmond, WA, USA). A histogram was generated and the cumulative score across all patients was calculated at each anatomic location and visualized using a radar chart to display the spatial distribution of edema cumulatively across all subjects.

Figure 1.

Scoring sheet used to grade the severity of fluid infiltration at 5 levels along the extremity was scored from 0–3, with 0 indicating the absence of fluid infiltration and 3 reflecting severe fluid infiltration (Illustration courtesy of Ryoko Hamaguchi, MD)

RESULTS

Eleven patients with MRI stage 1 upper extremity lymphedema were identified between January 2017 and January 2022. Ten patients (91%) were female, and one patient was male (9%). The average age of the overall cohort was 58 years, and the average BMI was 30 m/kg². One patient had (9%) primary upper extremity lymphedema and the remaining ten patients had secondary lymphedema (91%). Of those with secondary lymphedema (n=10), eight had breast cancer related lymphedema, one developed lymphedema following an episode of cellulitis, and one patient developed lymphedema following cosmetic breast reconstruction and brachioplasty. The average symptom duration of the cohort was 6.4 years.

An example case is shown in Figure 2. Graphical representations of edema distribution are shown in Figure 3. The hand was completely spared in all cases but one. The forearm was affected in nine cases (82%). Along the forearm, fluid infiltration both proximally and distally was concentrated in the ulnar forearm and to a lesser extent, the volar forearm. Notably, in all eleven cases (100%) the radial forearm was entirely unaffected. In the distal upper arm, fluid was primarily concentrated posteriorly and occasionally present medially. The proximal upper arm was only involved in one case, in which fluid was present medially.

Figure 2.

Example of fluid scoring on axial T2-weighted fat-suppressed MR images obtained at the five measured levels along the upper extremity in a patient with right upper extremity lymphedema.

Figure 3.

The distribution of edema at the level of the distal forearm (A), proximal forearm (B), distal upper arm (C), and proximal upper arm (D).

DISCUSSION

In this study we characterized spatial distribution of fluid in patients with MRI stage 1 upper extremity lymphedema. Fluid infiltration was concentrated in the ulnar forearm and the posterior distal upper arm, and with complete sparing of the radial forearm.

In all cases (n=11), the radial forearm was spared from edema. One possible explanation is a more robust lymphatic drainage at this location. We have previously observed that the radial forearm lymphatic channels are more likely to have a functional connection to the lateral upper arm pathway, which is postulated to be a compensatory route of lymphatic drainage after axillary lymph node dissection (Figure 4).^8–10 Radial forearm sparing on MRI may further support that a connection from the radial forearm channel to the lateral upper arm channel may protect patients from developing advanced disease.⁶

Figure 4.

Schematic of major posterior forearm lymphatic pathways and their most frequently observed connectivity to compensatory lymphatic pathways in the upper arm.

Along the forearm, fluid infiltration was most frequently seen along the ulnar aspect. The ulnar lymphatic channel is less likely to have a connection to the lateral upper arm pathway and is associated more with the tricipital lymphatic pathway, a compensatory route of lymphatic drainage.^11–13 However, the tricipital channel is less frequently observed, as shown in both in cadaveric dissections and in vivo.^11,14 We therefore propose that compromised or unfavorable anatomic variations of the tricipital pathway may lead to edema at the ulnar forearm. Gravity dependence has been postulated to play a role.¹⁵ However, this would not explain the distribution observed in our study, as we would have also expected a greater accumulation of fluid in the hands and distal extremities, but the hand was essentially spared.

In the distal upper arm, fluid was primarily concentrated posteriorly and occasionally medially. The proximal upper arm was only involved in one case, in which the fluid was present medially. Additionally, we propose that the distal posterior upper arm may be a particularly susceptible area to edema due to the relative lack of superficial lymphatic channels present in this area, when compared to the anterior upper arm.⁹ This corresponds to our clinic’s experience, where patients with very early-stage lymphedema complain of discomfort along the posterior upper arm, just proximal to the olecranon.

We found that the most frequent areas of fluid accumulation in upper extremity lymphedema, mainly the ulnar forearm and the posterior upper arm, align with the trajectory of the tricipital lymphatic pathway, adding support that unfavorable anatomical variations of the tricipital pathway may help explain this most common pattern of fluid distribution. These findings can help guide management of lymphedema at the earliest stage. For example, attention to the ulnar forearm and posterior upper arm during lymphedema surveillance of patients after lymphadenectomy may aid in detecting subclinical disease, resulting in earlier intervention and prevention or mitigation of disease progression. Moreover, it would be useful for lymphedema physical therapists to focus on vulnerable areas of the limb during manual lymphatic drainage in those with mild stage lymphedema. Surgical interventions may be modified to prevent fluid accumulation in vulnerable areas; for example, lymphatic surgeons may consider performing additional lymphovenous bypasses of ulnar forearm channels or transplantation of a lymph node flap to the ulnar aspect of the forearm.

This study is not without limitations. This study was observational, and a small number of patients were evaluated. Additionally, the MRI grading system is semi-qualitative and thus partially subjective. Finally, all but one patient had secondary lymphedema, and the conclusions may not be applicable to primary lymphedema.

CONCLUSION

In patients with early-stage lymphedema, fluid infiltration was concentrated along the ulnar forearm and the posterior aspect of the distal upper arm, with sparing of the radial forearm. This pattern of edema corresponds to key lymphatic drainage pathways and may be helpful in guiding therapy. This study also reflects the potential use of MRI in corroboration with other imaging modalities to map and understand lymphatic anatomy.