Authors

  • Prof. Markus L. Schneider
    Institute of Diagnostic and Interventional Radiology University Hospital Heidelberg, Heidelberg, Germany
  • Dr. Hossein R. Mirzaei
    Department of Medical Imaging, Tehran University of Medical Sciences, Tehran, Iran

DOI:

https://doi.org/10.71337/inlibrary.uz.ajbspi.104538

Keywords:

Lipedema Ultrasonography Qualitative Classification

Abstract

Lipedema, a chronic and progressive adipose tissue disorder, is characterized by disproportionate fat accumulation, primarily in the lower extremities, often leading to pain, bruising, and mobility impairment. Despite its significant prevalence and impact on quality of life, diagnosis remains challenging, frequently relying on clinical examination and patient history. Ultrasonography holds promise as a non-invasive diagnostic tool, offering insights into subcutaneous tissue characteristics. However, developing a standardized qualitative ultrasonographic classification for lipedema presents considerable challenges due to the heterogeneous nature of fat tissue, variability in disease presentation, and the subjective interpretation inherent in qualitative assessments. This article reviews the current diagnostic landscape of lipedema, explores the potential and limitations of ultrasonography, and critically examines the complexities involved in establishing a robust qualitative ultrasonographic classification. By outlining these challenges, we aim to guide future research towards more objective and standardized imaging criteria, ultimately improving the accuracy and consistency of lipedema diagnosis.


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VOLUME

Vol.05 Issue06 2025

PAGE NO.

1-7




Challenges in Developing a Qualitative Ultrasonographic
Classification for Lipedema

Prof. Markus L. Schneider

Institute of Diagnostic and Interventional Radiology University Hospital Heidelberg, Heidelberg, Germany

Dr. Hossein R. Mirzaei

Department of Medical Imaging, Tehran University of Medical Sciences, Tehran, Iran

Received:

03 April 2025;

Accepted:

02 May 2025;

Published:

01 June 2025

Abstract:

Lipedema, a chronic and progressive adipose tissue disorder, is characterized by disproportionate fat

accumulation, primarily in the lower extremities, often leading to pain, bruising, and mobility impairment. Despite
its significant prevalence and impact on quality of life, diagnosis remains challenging, frequently relying on clinical
examination and patient history. Ultrasonography holds promise as a non-invasive diagnostic tool, offering
insights into subcutaneous tissue characteristics. However, developing a standardized qualitative
ultrasonographic classification for lipedema presents considerable challenges due to the heterogeneous nature
of fat tissue, variability in disease presentation, and the subjective interpretation inherent in qualitative
assessments. This article reviews the current diagnostic landscape of lipedema, explores the potential and
limitations of ultrasonography, and critically examines the complexities involved in establishing a robust
qualitative ultrasonographic classification. By outlining these challenges, we aim to guide future research towards
more objective and standardized imaging criteria, ultimately improving the accuracy and consistency of lipedema
diagnosis.

Keywords:

Lipedema, Ultrasonography, Qualitative Classification, Diagnosis, Adipose Tissue, Chronic Disease,

Diagnostic Imaging.

Introduction:

Lipedema is a chronic, progressive

disorder of adipose tissue, predominantly affecting
women,

characterized

by

a

disproportionate

accumulation of fat, typically in the lower extremities,
from the hips to the ankles, while sparing the feet [2,
3]. This condition is often misdiagnosed as general
obesity or lymphedema, leading to delayed or
inappropriate treatment [2, 5]. Patients with lipedema
frequently experience pain, tenderness, easy bruising,
and impaired mobility, significantly impacting their
quality of life [2, 8]. The prevalence of lipedema is
substantial, with recent studies in Brazil indicating its
significant presence and associated risk factors [1].
Despite its widespread occurrence and debilitating
symptoms, lipedema remains under-recognized and
under-diagnosed globally, highlighting a critical unmet
need in clinical practice [7, 8].

The diagnosis of lipedema primarily relies on clinical
criteria, including specific fat distribution patterns, pain
upon palpation, easy bruising, and the absence of
pitting edema in the affected areas [3, 8]. However, the
subjective nature of these clinical assessments can lead
to diagnostic inconsistencies and delays. Objective
diagnostic tools are urgently needed to provide a more
definitive and standardized approach to identification.

Diagnostic medical imaging plays a crucial role in
modern medicine, offering valuable insights into
disease pathology [10]. Ultrasonography, in particular,
is a non-invasive, cost-effective, and readily available
imaging modality that has shown potential in
differentiating lipedema from other conditions like
obesity and lymphedema by visualizing subcutaneous
tissue characteristics [9]. Early research suggests that
specific ultrasound criteria, such as increased


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subcutaneous fat thickness, altered echogenicity, and
the presence of characteristic "snowstorm" or
"cobblestone" patterns, may aid in lipedema diagnosis
[9].

However, the development of a standardized and
widely

accepted

qualitative

ultrasonographic

classification for lipedema presents significant
challenges. The inherent variability in fat tissue
composition, the progressive nature of lipedema with
different stages, and the subjective interpretation of
qualitative ultrasound features contribute to these
complexities. This article aims to explore these
challenges in detail, reviewing the current state of
lipedema diagnosis, the promise and limitations of
ultrasonography, and the specific hurdles in
establishing a robust qualitative ultrasonographic
classification. By dissecting these issues, we hope to
contribute to a clearer understanding of the path
forward for improving diagnostic accuracy in lipedema.

Literature Review

Lipedema is a complex and often misunderstood
condition, distinct from general obesity and
lymphedema, yet frequently confounded with them [2,
5]. The lack of a definitive diagnostic test contributes
significantly to diagnostic delays and misdiagnosis,
impacting patient care [8].

2.1. Clinical Diagnosis and Differential Diagnosis:

The current standard of care for lipedema in the United
States and other regions relies heavily on clinical
examination [3, 8]. Key diagnostic features include:

Symmetrical,

disproportionate

fat

accumulation: Primarily affecting the legs (from hips to
ankles) and sometimes the arms, with a sharp
demarcation at the wrists and ankles, sparing the hands
and feet [2, 3].

Pain and Tenderness: Affected adipose tissue is

often painful to touch and can bruise easily [2, 8].

Negative Stemmer's Sign: The skin at the base

of the toes cannot be pinched and lifted, which is
typically positive in lymphedema [3].

Absence of Pitting Edema: In the early stages,

although secondary lymphedema can develop in later
stages [6].

Differentiating lipedema from obesity is crucial, as
lipedema fat is resistant to diet and exercise [2]. While
obesity can affect lymphatic function [4], lipedema is a
distinct pathological entity. Distinguishing it from
lymphedema,

which

involves

lymphatic

fluid

accumulation, is also vital for appropriate management
[6].

2.2. Role of Medical Imaging in Lipedema:

Given the diagnostic challenges, medical imaging has
been explored as a potential objective tool. Various
imaging modalities have been investigated:

Magnetic Resonance Imaging (MRI): Can

provide detailed anatomical information about fat
distribution and may show characteristic patterns in
lipedema fat, but it is expensive and not always readily
available [2].

Computed Tomography (CT): Also provides

detailed cross-sectional images but involves radiation
exposure, making it less suitable for routine diagnosis
[10, 11].

Lymphoscintigraphy: Useful for assessing

lymphatic function and differentiating lipedema from
primary or secondary lymphedema, but it is an invasive
procedure [4].

Dual-energy X-ray Absorptiometry (DXA): Can

quantify div composition and fat distribution but
does not provide detailed tissue characteristics.

2.3. Ultrasonography in Lipedema Diagnosis:

Ultrasonography is a non-invasive, radiation-free [FDA,
Cleveland Clinic, American Cancer Society], and
relatively inexpensive imaging technique that has
emerged as a promising tool for visualizing
subcutaneous tissue in lipedema [9]. Amato et al.
(2021) specifically proposed ultrasound criteria for
lipedema diagnosis, highlighting several key features
[9]:

Increased

Subcutaneous

Fat

Thickness:

Particularly in affected areas compared to unaffected
areas or control subjects.

Altered Echogenicity: Lipedema fat may exhibit

a more heterogeneous or "snowstorm" appearance
compared to normal fat, due to underlying fibrosis or
edema [9].

"Cobblestone" Pattern: Some studies describe

a characteristic "cobblestone" pattern, possibly related
to septal thickening or nodular fat lobules [9].

Dilated Blood Vessels/Lymphatics: Though less

consistently reported, some observations suggest
dilated vessels within the lipedema fat.

Absence of Dermal Thickening: Helping to

differentiate from lymphedema.

2.4. Challenges in Qualitative Ultrasonographic
Classification:

Despite these promising features, developing a
standardized qualitative ultrasonographic classification
for lipedema faces significant hurdles:

Subjectivity of Qualitative Descriptors: Terms

like "snowstorm" or "cobblestone" are subjective and


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can be open to varied interpretation among different
sonographers or clinicians [9]. This inter-observer
variability can reduce diagnostic consistency.

Heterogeneity of Lipedema Fat: Lipedema is a

progressive disease, and the structural characteristics
of the adipose tissue can vary depending on the stage
and individual patient. Early-stage lipedema might
show subtle changes, while later stages might exhibit
more pronounced fibrosis or nodularity, making a
single, fixed qualitative classification difficult [2, 3].

Overlap with Other Conditions: While

ultrasound can help differentiate, there can still be
some overlap in qualitative appearances between
lipedema, obesity (especially morbid obesity [4]), and
secondary lymphedema, particularly in advanced
stages [6].

Dependence on Equipment and Operator Skill:

The quality of ultrasound images and their
interpretation depend heavily on the ultrasound
machine's resolution and the sonographer's experience
and skill [10].

Lack of Standardized Protocols: There is

currently no widely accepted standardized protocol for
performing ultrasound examinations specifically for
lipedema, including parameters like probe frequency,
depth settings, or measurement points [9]. This lack of
standardization makes comparative studies and
universal classification difficult.

These challenges underscore the complexity of moving
from promising observations to a reliable, universally
accepted qualitative ultrasonographic classification for
lipedema.

METHODOLOGY

(This section will outline a hypothetical methodological
approach that researchers might undertake to address
the

challenges

of

developing

a

qualitative

ultrasonographic classification for lipedema. It will not
describe an actual experiment, but rather propose a
robust study design.)

To address the challenges in developing a qualitative
ultrasonographic classification for lipedema, a multi-
center, prospective, observational study with a focus
on inter-rater reliability and correlation with clinical
staging would be crucial.

3.1. Study Design and Participants:

Design: A prospective, observational study

with a cross-sectional component for initial
classification and a longitudinal component for tracking
disease progression and classification stability.

Participants: A large cohort of female patients

(N=500-1000) diagnosed with lipedema based on

established clinical criteria (e.g., S2K Guideline
Lipedema [3], Standard of Care for Lipedema in the
United States [8]). A control group of age- and BMI-
matched healthy women, and groups with general
obesity and secondary lymphedema, would also be
included for differential diagnosis comparison.
Participants would be recruited from multiple
specialized lipedema clinics to ensure diverse disease
presentations.

3.2. Data Collection:

Clinical Data: Comprehensive clinical data

would be collected for all participants, including:

o

Detailed medical history and physical

examination findings specific to lipedema (pain,
bruising, fat distribution, Stemmer's sign).

o

Clinical staging of lipedema (e.g., Stages I-

III/IV).

o

Anthropometric measurements (BMI, limb

circumferences, volume measurements).

o

Quality of life assessments.

Ultrasonography Data:

o

Standardized

Protocol

Development:

A

rigorous, standardized ultrasound protocol would be
developed collaboratively by expert sonographers and
lipedema specialists. This protocol would specify:

o

Ultrasound machine settings (e.g., probe frequency
(e.g., 7-15 MHz linear array), depth, gain).

o

Specific anatomical landmarks and measurement
points (e.g., thigh, calf, arm at defined intervals).

o

Standardized image acquisition techniques (e.g.,
consistent

pressure,

perpendicular

probe

orientation).

o

Image

Acquisition:

Two

independent,

experienced sonographers, blinded to clinical
diagnosis, would perform ultrasound examinations on
each participant using the standardized protocol.

o

Image

Parameters

for

Qualitative

Classification: Images would be acquired to evaluate:

Subcutaneous

Fat

Thickness:

Objective

measurement at standardized points.

Echogenicity Patterns: Qualitative descriptions of
fat

echogenicity

(e.g.,

homogeneous,

heterogeneous,

"snowstorm,"

"cobblestone,"

presence of fluid pockets, fibrosis). High-resolution
images of various tissue layers would be captured.

Presence and Characteristics of Septa/Nodules:
Qualitative description of fibrous septa, fat lobules,
and nodular formations.

Vascularity/Lymphatics: Presence of dilated vessels


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or lymphatics within the fat layer.

Digital Image Archiving: All ultrasound images

and clips would be digitally archived for subsequent
independent qualitative analysis.

3.3. Data Analysis:

Qualitative Classification Development:

o

A panel of expert sonographers and lipedema

specialists (blinded to patient clinical details) would
independently review a large, diverse set of ultrasound
images.

o

They would use a consensus-building process

to develop a preliminary qualitative classification
system based on reproducible visual patterns. This
might involve iterative discussions and refinement
based on initial inter-rater agreement assessments.

o

The classification would aim to describe

distinct patterns (e.g., "fine granular," "coarse
granular," "nodular," "fibrotic") and their potential
correlation with disease stage.

Inter-Rater

Reliability:

The

developed

qualitative classification system would be applied by
multiple independent, blinded expert raters to a subset
of the archived ultrasound images. Kappa statistics and
intraclass correlation coefficients (ICCs) would be used
to assess inter-rater agreement on the qualitative
descriptors and proposed classification categories.

Correlation with Clinical Staging: The finalized

qualitative ultrasonographic classifications would be
correlated with the established clinical stages of
lipedema using appropriate statistical methods (e.g.,
Chi-square, regression analysis). The aim is to
determine if specific qualitative ultrasound patterns
are consistently associated with particular clinical
stages.

Differential Diagnosis Efficacy: Ultrasound

findings from lipedema patients would be compared
with those from obesity and lymphedema control
groups to identify unique qualitative features that aid
in differential diagnosis.

3.4. Ethical Considerations:

Ethical approval would be obtained from all
participating institutional review boards. Informed
consent would be secured from all participants,
ensuring confidentiality and voluntary participation.
Given that ultrasound imaging does not involve ionizing
radiation, the risks associated with the imaging
procedure itself are minimal [FDA, Cleveland Clinic,

American Cancer Society]. However, the ethical
implications of using imaging for non-medical reasons
or by untrained users would be considered in the
broader context [Cleveland Clinic].

RESULTS

(This section presents hypothetical results based on the
common findings and challenges encountered in
developing qualitative classifications for complex
medical conditions, particularly in imaging.)

The hypothetical study designed to develop and
validate a qualitative ultrasonographic classification for
lipedema would likely yield the following results,
highlighting both potential and persistent challenges:

Stages and features of lipedema. (a) to (f): Front and
back pictures of women with lipedema Stages 1 to 3.
Staging references the legs, however women pictured
also have arm involvement. Stage 1 skin has a smooth
texture with subdermal pebblelike feel due to
underlying loose connective tissue fibrosis. Lipedema
Stage 2 women have more lipedema tissue than
women with Stage 1 and skin dimpling due to
progressed fibrotic changes and excess tissue. Palpable
nodules may be more numerous and larger. Note the
full Achilles sulci in pictures (d) to (f). In Lipedema Stage
2 arms, the tissue begins to hang off the arm and full
arm involvement shows a more pronounced wrist cuff.
Lipedema Stage 3 features increased lipedema tissue
more fibrotic in texture with numerous large
subdermal nodules and overhanding lobules of tissue.
Patient (e) and (f) has lipedema, non-lipedema obesity
and lipolymphedema. Types I to V describe the
locations of lipedema tissue. Type I, lipedema tissue is
present under the umbilicus and over hips and
buttocks, Type II, under the umbilicus to knees (a, b),
Type III, under the umbilicus to ankles (c to f), Type IV,
arms (a to f) and Type V, lower legs (not shown). A
tissue cuff at the ankle or wrist may be present in all
stages. (g): Lipedema tissue overhangs the elbow. (h):
Lipedema tissue often hangs well below the arm due to
loss of elasticity and heaviness of the tissue. (i): Livedo
reticularis is often a feature of lipedema. (j): Close view
of tissue filling the Achilles sulci. (k): Close view of a
column type lipedema leg with an obvious ankle cuff.
(l): An ankle of a woman with lipedema without an
ankle cuff (compare to (k)). (m): Pronation of the ankle
commonly found in women with lipedema. Consent
was obtained for use of all photos. LCT: loose
connective tissue.


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4.1. Identification of Common Ultrasonographic
Features in Lipedema:

The initial image review by expert sonographers would
confirm the presence of several recurring qualitative
features in lipedema adipose tissue, consistent with
previous observations:

Increased

Subcutaneous

Fat

Thickness:

Quantifiable measurements would show significantly
greater fat thickness in affected limbs of lipedema
patients compared to control groups, particularly at
specific anatomical sites (e.g., inner thigh, medial calf).

Heterogeneous

Echogenicity:

A

highly

prevalent finding would be the heterogeneous
appearance of subcutaneous fat, varying from a
"snowstorm" or "ground glass" texture in some areas,
potentially indicative of edema within the fat, to more
areas of increased echogenicity suggesting fibrosis.

"Cobblestone" Pattern: This characteristic

pattern, representing enlarged fat lobules separated by
thickened septa, would be identifiable in a considerable
subset of lipedema patients, particularly in more
advanced stages.

Presence of Nodules: Palpable nodules would

correlate with distinct hyperechoic structures within
the fat layer, often with irregular shapes.

Dilated

Lymphatics/Vessels:

While

less

consistently visualized, some images would show
evidence of dilated lymphatic vessels or small blood
vessels within the subcutaneous fat, possibly due to
underlying inflammation or lymphatic dysfunction.

4.2.

Challenges

in

Qualitative

Classification

Development:

Despite identifying common features, the process of
developing a qualitative classification based on these
features would face significant hurdles:

Inter-Rater

Variability

in

Qualitative

Descriptors: When multiple independent raters apply
subjective terms like "snowstorm" or "cobblestone" to
the same images, inter-rater reliability (Kappa
coefficients) would be only moderate (e.g., Kappa = 0.4-
0.6), indicating a lack of strong consensus in subjective
interpretation. This highlights the inherent ambiguity
of purely qualitative descriptions.

Continuum vs. Discrete Categories: The

observed ultrasonographic changes often exist along a
continuum rather than falling into clear, discrete
categories. Early-stage lipedema might show subtle
heterogeneity, gradually progressing to more
pronounced fibrosis and nodularity. Attempting to
force these continuous changes into a few distinct
qualitative stages would prove challenging, leading to
boundary disputes among raters.

Overlap with Other Conditions: While

quantitative fat thickness might differ, the qualitative
appearance of fat in some lipedema patients (especially
those with secondary lymphedema or severe obesity)
could still overlap with the appearance of fat in control
groups or those with other conditions, making
definitive qualitative differentiation difficult. For
instance, severe obesity can also present with
heterogeneous fat patterns.


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Influence of Probe Pressure and Technique:

Despite a standardized protocol, subtle variations in
probe pressure during image acquisition could affect
the perceived echogenicity and compressibility of the
fat, influencing qualitative interpretation.

4.3. Limited Correlation with Clinical Staging:

The attempt to correlate proposed qualitative
ultrasonographic categories with established clinical
stages of lipedema would yield only moderate or weak
associations. While patients with clinically advanced
lipedema (Stage III/IV) might consistently exhibit more
fibrotic or nodular patterns, and early-stage patients
(Stage I) might show more subtle heterogeneity or
"snowstorm"

patterns,

a

clear,

one-to-one

correspondence for all stages would not be consistently
evident. This indicates that a purely qualitative
ultrasonographic classification might not fully capture
the clinical heterogeneity of lipedema or may be too
broad to accurately reflect subtle stage differences.

In summary, while ultrasonography can identify several
characteristic features of lipedema, the results suggest
significant challenges in creating a robust and reliable
qualitative ultrasonographic classification due to the
subjective nature of visual interpretation and the
heterogeneous presentation of the disease.

DISCUSSION

The findings from this hypothetical study highlight the
persistent difficulties in developing a robust qualitative
ultrasonographic classification for lipedema. While
ultrasonography undeniably offers valuable insights
into the subcutaneous adipose tissue characteristics in
lipedema, and can distinguish it from normal fat and
even obesity [9], translating these observations into
universally reproducible qualitative categories remains
a significant hurdle.

The observed "inter-rater variability in qualitative
descriptors" is a central challenge. Terms like
"snowstorm" or "cobblestone" [9], while evocative, are
inherently subjective. What one sonographer perceives
as a distinct "cobblestone" pattern, another might
interpret as generalized heterogeneity. This lack of
precise, objective definitions leads to inconsistencies in
diagnosis and hinders the standardization needed for
widespread clinical application and research. It
reinforces the difficulty of achieving high reliability with
purely qualitative assessments in medical imaging [10].
To mitigate this, future efforts must move towards
more objective, quantifiable parameters, possibly
incorporating texture analysis algorithms or advanced
imaging techniques to characterize fat tissue.

The "continuum vs. discrete categories" issue further
complicates classification. Lipedema is a progressive

disorder [2, 3], meaning its ultrasonographic
appearance likely changes subtly over time and across
different stages. Attempting to fit this dynamic
spectrum into a limited number of static qualitative
categories may oversimplify the disease's complexity
and lead to misclassification. A more effective
classification might require a continuous scoring
system or a multi-parametric approach that considers
not just the "pattern" but also the severity of changes
and the presence of associated features (e.g., septal
thickness, vascularity).

The "overlap with other conditions," particularly severe
obesity and secondary lymphedema, is another critical
point. While ultrasound can help differentiate, the
qualitative appearance of fat in these conditions might,
at times, mimic certain lipedema features [4, 6]. This
necessitates

careful

correlation

with

clinical

examination and patient history, emphasizing that
ultrasound is an adjunctive tool rather than a
standalone diagnostic arbiter for lipedema. Future
research should focus on identifying highly specific
ultrasonographic "signatures" for lipedema that are
truly unique to the condition and resistant to
confounders.

The "influence of probe pressure and technique"
highlights

the

operator-dependent

nature

of

ultrasound. Even with standardized protocols, subtle
variations can affect image quality and interpretation.
This underscores the need for extensive training and
certification for sonographers involved in lipedema
assessment to ensure consistency and accuracy. Efforts
to reduce low-value imaging [11] also implicitly
highlight the need for clear diagnostic utility and
standardization.

Ultimately, while qualitative ultrasonography offers
promising avenues for lipedema diagnosis, its current
limitations prevent the establishment of a robust,
universally accepted classification. Moving forward,
research should focus on:

1.

Developing

Quantitative

Ultrasound

Parameters: Moving beyond subjective descriptors to
measure specific parameters like fat lobule size, septal
thickness, and tissue compressibility using advanced
ultrasound modalities (e.g., elastography).

2.

Integrating

Multi-parametric

Analysis:

Combining multiple qualitative and quantitative
ultrasound features into a comprehensive scoring
system rather than relying on a single qualitative
pattern.

3.

Artificial

Intelligence/Machine

Learning:

Utilizing AI algorithms to analyze ultrasound images for
subtle patterns not easily discernible by the human
eye, potentially leading to more objective and


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consistent classifications.

4.

Longitudinal

Studies:

Tracking

ultrasonographic changes over time in lipedema
patients to better understand disease progression and
refine stage-specific imaging criteria.

By addressing these challenges, the field can progress
towards a more objective, reliable, and clinically useful
ultrasonographic classification for lipedema, ultimately
facilitating earlier and more accurate diagnosis for
millions of affected individuals.

CONCLUSION

The development of a standardized qualitative
ultrasonographic classification for lipedema presents
significant challenges stemming from the subjective
nature of visual interpretation, the inherent
heterogeneity and progressive nature of the disease,
and potential overlaps with other conditions. While
ultrasonography offers valuable, non-invasive insights
into subcutaneous adipose tissue, the current
qualitative descriptors lack the precision and
reproducibility needed for a universal classification
system.

Despite these hurdles, the potential of ultrasound as a
diagnostic adjunct for lipedema remains high. Future
efforts must pivot towards more objective, quantitative
ultrasonographic parameters, potentially leveraging
advanced imaging techniques and artificial intelligence
to overcome subjective biases. By striving for a robust
and reliable imaging classification, the medical
community can significantly improve the accuracy and
consistency of lipedema diagnosis, ultimately leading
to earlier intervention and better outcomes for
affected patients.

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75,

121-125.

https://doi.org/10.18043/ncm.75.2.121

Kjelle, E., Andersen, E.R., Soril, L.J.J., van Bodegom-Vos,
L. and Hofmann, B.M. (2021) Interventions to Reduce
Low-Value

Imaging

A

Systematic

Review

of

Interventions and Outcomes. BMC Health Services
Research,

21,

Article

No.

983.

https://doi.org/10.1186/s12913-021-07004-z

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