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PERMANYERwww.permanyer.com
www.analesderadiologiamexico.com Anales de Radiología México.
2017;16(2):111-120
1665-2118/©2017 Sociedad Mexicana de Radiologia e Imagen, AC.
Publicado por Permanyer México SA de CV. Este es un artículo Open
Access bajo la licencia CC BY-NC-ND
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
ABSTRACT
Correspondence to: María Teresa Moreno-Ramírez Dr. Balmis 148,
Col. Doctores, 06700 Ciudad de México, México E-mail:
[email protected]
Received in original form: 18-01-2017 Accepted in final form:
27-05-2017
Characterization of the most common liver lesions by
diffusionCaracterización de las lesiones hepáticas más comunes por
medio
de difusiónM.T. Moreno-Ramírez1, M.C. Amezcua-Herrera2 and A.E.
Vega-Gutiérrez3
1Médico Residente de Alta Especialidad en Resonancia Magnética
en el Departamento de Radiología e Imagen; 2Jefe de Servicio del
Área de Resonancia Magnética, Adscrito al Servicio de Radiología e
Imagen; 3Médico Radiólogo Adscrito al Departamento de Radiología e
Imagen. Hospital General de México Eduardo Liceaga, Ciudad de
México, México
ORIGINAL ARTICLE
This article must be quoted as: Moreno-Ramírez MT,
Amezcua-Herrera MC, Vega-Gutiérrez AE. Caracterización de las
lesiones hepáticas más comunes por medio de difusión. Anales de
Radiología México 2017;16(2):111-120.
http://www.analesderadiologiamexico.comhttp://creativecommons.org/licenses/by-nc-nd/4.0/
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Anales de Radiología México. 2017;16
INTRODUCTION
Diffusion-weighted images in magnetic resonance (RM) are a
technique that first started for the diagnosis of acute brain
in-farcts. Stejskal and Tanner were the first to use diffusion
properties in RM sequences in 1961, Le Bihan et al. created
the first brain magnetic resonance imaging (MRI) diffusion image in
1986, and Warach et al. were the first to use this technique
in a brain infarct in 1992; however, the application of this
tech-nique to study abdominal disease is relative-ly recent. The
typical limitation of diffusion in an abdominal MRI has been the
image degradation due to respiratory movements, so synchronization
with breathing and synchro-nization with the heart can be useful
when the left liver lobe is to be scanned, to avoid artifacts due
to heart movements. However, technological advances in MRI have led
to the application of diffusion in studying abdomi-nal disease,
particularly for the diagnosis of liver lesions1,2. Recently, the
possibility of us-ing diffusion for the study of diseases outside
the nervous system has been shown, especial-ly neck and abdomen, to
which other appli-cations have been found in chest, breast, and
muscle-skeletal system. Oncological applica-tions are among those
that have attracted the greatest interest for tumor diagnosis and
follow-up1,2.
Diffusion is the physical property that de-scribes Brownian
movement or random movement of water molecules in tissue, as a
response to thermal energy1,3. The human body is made of 75% water,
located in three compartments: intravascular, intracellular, and
extracellular. The diffusion sequence is sensitive to detection of
the movement of wa-ter molecules in these compartments at a
mi-croscopic level, but the movement of water molecules in the
extracellular space is the one that is of most interest for the
study of tumor lesions. The higher or lower rate of the move-ment
of water molecules in the extracellular space will be essentially
conditioned by the amount of cells, the integrity of membranes, and
the viscosity of tissue. Thus, in tissue with a small amount of
cellularity such as in benign tumors or ruptured membranes such as
tumors with necrosis, the water molecules move easily, which is
known as free diffu-sion; in tissue with great cellularity (such as
in malignant tumors), the movement of water molecules is limited,
and therefore, diffusion will be restricted4-6. It is important to
empha-size that resonance is the only method that can detect and
measure molecular diffusion in vivo7.
Every time, we use the diffusion sequence, and in practice, we
use two values of “b”: 0 s/mm2 and between 400 and
1000 s/mm2.
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common liver lesions by diffusion
In general, the greater the value of B, the greater the
attenuation of water molecules. However, it is necessary to
understand that the signal intensity that we see in the diffu-sion
sequence is a mixture of difussion as such and the T2 relaxation
time of tissue. This T2 effect, which may be confused
with restriction to diffusion, is called
“shine-through.”2,8-10
To characterize tumors in the liver, it is rec-ommended to use B
values between 0 and 600 s/mm2. The visual qualitative
analysis of diffusion tends to be enough for differentia-tion
between solid and cystic lesions, but to discriminate between
different solid lesions, we need to quantify diffusion values of
ap-parent diffusion coefficient. The qualitative assessment of
diffusion is useful for screen-ing and characterization of disease
by observ-ing the attenuation of the differential signal among
tissues in RM diffuse images.
Cell tissue such as tumors or abscesses will show restricted
diffusion and apparently low-er diffusion coefficient values;
cystic or ne-crotic tissue will show a greater attenuation of
signal in diffusion images and also higher values of apparent
diffusion coefficient that provides a quantitative measure,
regardless of the magnetic field that measures the mi-croscopic
displacement of the water mole-cules. It is possible to determine
the value of apparent diffusion coefficient in a given re-gion by
choosing a region of interest. In the apparent diffusion
coefficient map, we can calculate the capacity of diffusion in
specific tissue areas. If diffusion is restricted, the co-efficient
value is low, and if diffusion is facil-itated, the value will be
high2,4,11. One of the problems in qualitative analysis is that
the
signal we see depends not only on water dif-fusion but also the
T2 relaxation time. When B values are low, the image has a higher
po-tentiated T2, and when B values are high, the sequence is more
potentiated in diffusion9,12,13.
The liver may have a wide range of solid lesions, either benign
or malignant. The de-tection, characterization, and accurate
differ-entiation of these have always been one of the objectives of
the different imaging methods. In RM, the characterization of these
lesions is based on their morphology, signal intensity in the
different sequences, and their behavior with paramagnetic contrast
(gadolinium). Furthermore, specific contrast agents have been used
that are not easily available in our country due to their high
cost. However, even in the usual test protocols, there are still
cas-es where it is not possible to have adequate discrimination
between benign and malig-nant liver lesions. Currently, diffusion
se-quences with different B values are acquired, to discriminate
between benign and malig-nant liver lesions, without the need of
using contrast agents, mainly in patients with kid-ney disease.
Diffusion is considered an im-portant tool for the diagnosis of
liver lesions as a complementary and additional sequence to the
customary test protocol. It is important for radiologists to
familiarize themselves with the technique and to use it to enhance
their knowledge and facilitate its clinical applica-tion. This
study was conducted to determine the qualitative values of
diffusion for the de-tection, characterization, and differentiation
of liver lesions.
RM is a non-invasive diagnostic method of general use, with
adequate availability in the clinical practice of our setting that
can be
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performed in wide population groups. It provides morphological,
qualitative, and quantitative information in this context; RM
diffusion sequences play an important grow-ing role by studying
molecular behavior, one of the future pillars of diagnostic
imaging. Our goal is to show that malignant liver le-sions have
diffusion restriction corroborated in sequences of apparent
diffusion coefficient, and for that purpose, we reviewed the role
of diffusion for detection, characterization, and discrimination of
liver lesions; we evaluate its useful role in benign and malignant
liver lesions.
MATERIALS AND METHODS
This is a descriptive, retrospective, cross-sec-tional study.
The sample size estimate was according to “convenience” from March
2014 to September 2016, in patients of the Hospital General de
México Eduardo Liceaga, who un-derwent an MRI of the abdomen with
diffu-sion basic sequence to identify and character-ize liver
lesions. A retrospective review was done in the PACS-RIS system and
the scans with a diagnosis of liver lesion were selected, imaging
findings were assessed, and the be-havior of lesions in the
different sequences was reviewed, especially the diffusion
behav-ior and the apparent diffusion coefficient. Pa-tients over
18 years of age were included, and all those in whom the
outcome of the studied liver lesion could not be followed when they
had a diffusion MRI of the abdomen in the hospital, patients under
18 years of age were excluded and all those in whom the outcome of
the lesion could not be followed in their scan or that had no
histopathology sample. The conventional and diffusion MRI was
performed using a Siemens® Avanto 1.5 Tesla, with diffusion
factors (B) of different sensiti-zation grades (50, 400, and
800 s/mm2).
The conventional MRI studies were interpret-ed by a radiologist
with 10 years of experi-ence in MRI. The final diagnosis of
the nature of the lesions was determined by their char-acteristics
in ultrasonography, multisection computed tomography, and MRI with
and without IV contrast, aside from the course of the benign
lesions that had biopsies. The vari-ables considered in our study
were age, gen-der, number of lesions (1, 2, 3, 5, and > 10),
size of the lesion (< 1 cm, 1-3 cm, > 5 cm,
and > 10 cm), morphology of the lesion (round, oval, or
geographical), borders of the lesion (lobulated, regular,
irregular, or ill-defined), signal intensity in the T1 and T2
sequences, diffusion, and apparent diffusion coefficient
(hypointense, isointense, and hyperintense). The patients included
in the study were clas-sified into two independent groups: with
be-nign or malignant lesions, and a descriptive statistical method
was used for the variables of interest.
RESULTS
Fifty-five patients were found who were in-cluded in the
established protocol for the de-tection and characterization of
liver lesions; nine patients were excluded for different rea-sons;
five patients did not have liver lesions, and in four patients, the
nature of the lesion was not possible to be confirmed. The cohort
included was made of 48 patients: 22 males (45.8%) and
26 females (54.1%). The mean age was 53.3 years (range
from 19 to 80 years). Of the 48 patients with liver
lesions, 22 were
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common liver lesions by diffusion
benign (45%) and 26 had malignant histopathology (54%): 11
metastases, 7 hepa-toparcinomas, 1 embryonic sarcoma, 2
gall-bladder tumors, 4 cholangiocarcinomas, and 1 neuroendocrine
tumor. Of the 22 benign lesions, 7 were abscesses, 5 hemangiomas,
5 regenerative nodules, 3 cysts, 1 hamartoma, and 1 polycystic
disease.
Concerning the number of lesions found, 28 patients had
only one lesion (58.3%), four had two lesions (8.3%), three
patients had three lesions (6.2%), four had 5 lesions (8.3%), and
only nine of them (18.7%) had more than 10 lesions; most of the
lesions had round shape (68.7%), 13 patients had oval
morphol-ogy, and only 1 had geographic appearance. In regard to the
borders of the lesions, 20 were described as lobulated, 17 had
regular border, 8 had irregular borders, and 3 had ill-defined
borders; the ill-defined and lobu-lated borders were directly
associated with the histopathology reports of metastases. The
smallest of the lesions detected was 0.6 cm and the largest
had 21 cm in the longest axis.
In T1-weighted sequences, most of the lesions (35) had low
signal intensity, the remaining lesions (12) had high signal
intensity, and one was isointense. Most of the lesions also showed
increased signal intensity in diffusion se-quences (37) and the
remaining lesions had decreased signal intensity (11)
[Table 1]. Of the 37 lesions that had diffusion restriction,
only 20 were real restrictions corroborated by the low signal
intensity of the apparent diffusion coefficient; of them, 10 were
metastases, 5 were hepatocarcinomas, 1 sarcoma,
3 cholangiosar-comas, and 1 neuroendocrine tumor, showing
diffusion restriction with B values over 400 and
increased signal intensity in B values at 800.
There were 17 lesions that simulated restricted diffusion, known
as T2 effect or shine through effect, identified with an apparent
diffusion coefficient map, where the signal is increased,
indicating that the diffusion is not real. This happened in
7 abscess cases, 3 cystic lesions, 4 hemangiomas, 2
regenerative nodules, and one case of liver polycystosis. Examples
of the most representative lesions and their respec-tive findings
are as follows.
Liver cysts
A simple cyst is a very common lesion; the incidence increases
significantly in congenital diseases such as polycystic kidney
disease or Von Hippel–Lindau disease. Their MRI ap-pearance is of
round morphology, well-out-lined borders, an approximate mean size
of 1-3 cm, showing low signal intensity in T1 and high signal
intensity in T2, with peripheral en-hancement following contrast
administration; no restriction was found and their appearance was
of low signal intensity in apparent diffu-sion coefficient. When
they present with diffu-sion restriction, it is due to their high
protein content or in cases with bleeding (Fig. 1).
Hepatocellular carcinomas
Hepatocellular carcinomas are variable, and they may be round,
oval, amorphous, with lobulated and imprecise borders, ranging
in
Table 1. Diffusion‑weighted lesions
Intensity with diffusion sequences n = 48
Decreased signal intensity 11
Increased signal intensity 37
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size from 4 to 14 cm, with low signal inten-sity,
isointense, or with high signal intensity in T1 and T2. High signal
intensity in T2 has greater specificity in the diagnostic scan of a
malignant nodule in cirrhotic liver, using non-contrast sequences;
following intrave-nous gadolinium injection, the early enhance-ment
of these lesions is noted, which is con-sidered as highly
suspicious of malignancy. They generally present with diffusion
restric-tion and low signal intensity in the apparent diffusion
coefficient. There are cases associ-ated with broad areas of
necrosis where it is possible that the diffusion restriction is not
visualized (Fig. 2).
Angiosarcoma
Angiosarcomas are high-grade vascular neo-plasms, with multiple
patterns of liver
growth. A large size single tumor stood out, round, with
regular and well-defined bor-ders, with satellite nodules and
multinodular shape. Central bleeding and necrosis are common. On
MRI, peripheral enhancement patterns were detected, and tumor
nodules are of low signal intensity in potentiated T1 sequences and
with moderate-high signal in-tensity in T2 (Fig. 3).
Metastasis
Multiple round and oval lesions were noted, 0.6-7 cm, of
multilobulated irregular borders. Lesions were sometimes confluent,
forming large tumors, and they could replace the liv-er parenchyma.
On MRI, they had low signal intensity on T1, frequently associated
to in-ternal bleeding with hyperintense internal foci; on T2, they
had intermediate signal in-tensity similar to the spleen, with a
hy-pointense halo; most had peripheral enhance-ment following
contrast administration, associated with diffusion restriction and
low signal intensity in the apparent diffusion co-efficient (Figs.
4 and 5).
Hemangiomas
Single or multiple lesions, with amorphous appearance, partially
outlined borders, vari-ous appearances in the different sequences,
during T1 they are frequently hyperintense as well as in T2. They
showed diffusion re-striction and heterogeneous behavior in the
apparent diffusion coefficient following con-trast administration
enhancement is uniform, intense, and persistent in late phases
(Fig. 6).
Figure 1. T2‑weighted sequences on T2 (A-C) coronal
sections (D) axial section. Multiple, round, diffuse liver and
renal lesions, decreased signal intensity on T1 and increased
signal intensity on T2; without contrast enhancement, associated to
different lesions with the same features in both kidneys. Patient
with polycytosis.
A
C
B
D
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common liver lesions by diffusion
Figure 3. (A-B) T1‑fat‑supressed coronal sequences;
(C) T1 axial sequence; (D) T2 axial sequence. Single
large lesion, regular and delineated borders, with a large amount
of internal fat and necrosis, associated to hyperintense peripheral
mural nodules.
A
C
B
D
Figure 4. (A) T1‑weighted sequence; (B) T2‑weighted
sequence; (C) diffusion; (D) ADC. Multiple, round, hypointense
lesions on T1, mildly hyperintense on T2, with diffusion
restriction and hypointense on ADC. Lesions corresponding to a
moderately differentiated colon adenocarcinoma.
A
C
B
D
Figure 2. Nodular round lesion, located in the VI liver
segment. (A) Increased signal intensity on T1; (B) decreased signal
intensity on T2; (C) heterogeneous restricted diffusion signal; (D)
lesions with low and high signal intensity ADC; (E) early and
uniform enhancement after contrast administration;
(F) histopathological confirmation.
D
CB
F
A
E
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Neuroendocrine tumors
We found them in a young patient with mul-tiple liver lesions,
with a round and oval
shape, lobulated borders, distributed in both liver lobes, of
uniform appearance, with solid and cystic lesions and heterogeneous
behav-ior in T1 and T2, partial restriction of lesions
Figure 5. Single, round lesion of irregular borders. (A)
Hypointense on T1; (B) hyperintense on T2: (C) with diffusion
restriction: (D) hypointense with ADC; (E) peripheral
enhancement; (F) the lesion corresponded to breast cancer
metastasis.
A
D
B
E
C
F
Figure 6. Behavior of the hemangioma. (A) hyperintense on
T1 because of its blood component; (B and D) hyperintense on T2; (C
and E) delayed enhancement after contrast administration.
A
C D E
B
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predominantly in the solid behavior, corrob-orated in the
apparent diffusion coefficient and strong enhancement with passage
of con-trast (Fig. 7).
DISCUSSION
In the assessment of liver lesions, MRI plays a valuable role,
due to its high resolution when images are obtained and without
radi-ation. Currently, new sequences such as dif-fusion are used to
obtain a better yield and helped to characterize the lesions for
their proper management; images are, especially, useful in patients
with kidney failure because gadolinium cannot be used and also in
patients who are allergic to contrast and who cannot have prolonged
apnea during image acquisition2,4,11. Diffusion sequences provide
quantification of water noninvasively;
therefore, they give functional information about the tissue
composition other than the morphological information obtained in
con-ventional sequences. The qualitative values of the apparent
diffusion coefficient correlate with the diffusion value14.
Nowadays, diffu-sion can be used for the whole human body,
particularly in liver scans, with the benefit of fast acquisition
and getting qualitative and quantitative information of the
lesion5.
Our results are similar to those obtained by other authors and
show that the high appar-ent diffusion coefficient values are seen
in benign lesions such as cyst or hemangiomas. Like these authors,
we also show that the ap-parent diffusion coefficient values of
heman-giomas are lower than those of cysts and higher than
hepatocarcinomas and metastases. This confirms the theory that
solid lesions have lower apparent diffusion coefficient due
Figure 7. Multiple lesions with heterogeneous behavior in
all sequences. (A and C) hypointense and hyperintense on T1;
(B) hyperintense on T2; (D) diffusion restriction; (E)
confirmed with ADC; (F) corresponding to a neuroendocrine
tumor.
A
D
B
E
C
F
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to their cellularity component that restricts diffusion of water
molecules. Hemangiomas do not have a pure liquid component but a
vascular endothelial content, fibrous septa, and blood. These
elements restrict the water movement and explain the lower apparent
diffusion coefficient values with respect to that of
cysts2,8,12.
A solid lesion defines its nature (solid or cys-tic) by means of
visual assessment of diffu-sion sequences, but to characterize a
solid lesion, it is necessary to note its morphology and behavior
in the different sequences. In malignant lesions, the diffusion
sequences al-low to differentiate the behavior of the tumor, cyst,
or necrosis of the solid component5,9. It is necessary to
characterize malignant and benign lesions, and sometimes, it is
extreme-ly difficult without the use of contrast. Our study, as
many others, suggests that the be-nign lesions have an apparent
diffusion coef-ficient value that is higher than in malignant
lesions. We obtained statistically significant results to
discriminate benign from malig-nant lesions3.
CONCLUSION
The diffusion sequence is useful to discrimi-nate benign from
malignant liver lesions. It is the most important diagnostic test
after dy-namic study following intravenous contrast administration
in the study of liver lesions us-ing MRI. Therefore, it is a good
option for patients who cannot be given intravenous con-trast.
These results show that the qualitative
assessment of diffusion helps to distinguish solid and cystic
lesions and also to determine if the lesions have a benign or
malignant be-havior. Nevertheless, with the use of only qualitative
assessment, it is not possible to specifically determine the type
of malignant lesion, so it is important to correlate the
mor-phological findings, the number of lesions, and the clinical
characteristics of each patient to be able to give an accurate
diagnosis.
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