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Improved Differentiation of Benign and Malignant Lymphadenopathy in Patients With Cutaneous Melanoma by Contrast-Enhanced Color Doppler Sonography
Monika-Hildegard Schmid-Wendtner, MD;
Karin Partscht, MD;
Hans Christian Korting, MD;
Matthias Volkenandt, MD
Arch Dermatol. 2002;138:491-497.
ABSTRACT
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Objective To evaluate whether administration of a D-galactose–based signal
enhancer is useful in color Doppler sonography (CDS) for better detection
of vascularity patterns, which may help to differentiate malignant from benign
lymph nodes in patients with cutaneous melanomas.
Design Comparison of B-mode sonography, native CDS, and signal-enhanced CDS.
Setting Department of Dermatology and Allergology, Ludwig-Maximilians-University,
Munich, Germany.
Patients Twenty examinations in 19 patients (median age, 60 years; 10 men) who
presented with echo-poor structures suggestive of lymphadenopathy in B-mode
sonography during follow-up for cutaneous melanomas.
Interventions Histopathologic and follow-up examinations; documentation by color prints.
Main Outcome Measures Frequency of detection and description of different lymph node vascularity
patterns in signal-enhanced CDS.
Results Signal-enhanced CDS revealed additional information about vascularization
of lymph node metastases, reactive lymph nodes, hematomas, and seromas, which
was helpful for the differential diagnosis in 15 of 20 examinations. For lymph
node metastases, signal enhancement facilitated the detection of accessory
peripheral vessels in most investigations. Concerning reactive lymph nodes,
hilar vessels in part with branching to the lymph node periphery could be
identified only after application of the contrast enhancer in most patients.
Quantitative variables could not be measured in all cases and did not help
to differentiate between malignant and reactive lymph nodes.
Conclusions Administration of a D-galactose–based signal enhancer for CDS
in patients with cutaneous melanomas can help to differentiate malignant from
reactive lymph nodes, hematomas, or seromas. However, these promising results
require confirmation in a prospective multicenter study.
INTRODUCTION
THE PROGNOSIS of patients with cutaneous melanomas primarily depends
on the tumor thickness at the time of diagnosis. Whereas patients with malignant
melanomas with a tumor thickness of 0.75 mm or less are cured with high probability
by surgical excision of the tumor, the prognosis is worse for patients with
thicker melanomas.1-2 In these
patients, the 10-year survival rate decreases markedly owing to development
of metastases.1 Regional lymph nodes are known
to be the first site of disease progression in most patients, and the number
of lymph node metastases are reported to be important for subsequent recurrence
and prolonged survival.3 For this reason, early
detection of lymph node metastases may be of special value in the follow-up
of patients with cutaneous melanoma. B-mode sonography has repeatedly been
reported to alter the management of patients with cutaneous melanomas by detection
of impalpable metastases in lymphatic drainage areas and regional lymph nodes.4-5 Moreover, color Doppler sonography
(CDS) has been shown to give additional diagnostic information because of
the detection of characteristic vascularization patterns in some, mostly enlarged,
malignant and reactive lymph nodes.6 The current
prospective study was performed to evaluate whether application of a D-galactose–based
contrast enhancer, routinely used in cardiology, for example, improved the
visualization of vascularization pattern in echo-poor structures suggestive
of lymphadenopathy detected by B-mode sonography in patients with cutaneous
melanomas.
PATIENTS AND METHODS
PATIENTS
A total of 19 patients (10 men and 9 women) seen during follow-up after
complete resection of invasive cutaneous malignant melanoma were prospectively
included in this study between April 1, 2000, and October 31, 2000, at the
Department of Dermatology and Allergology, University of Munich. For all patients,
written consent was obtained. Complete follow-up was at least 5 months in
all patients.
Age range of the patients was 23 to 78 years (mean, 57 years; median,
60 years). Patient characteristics are listed in Table 1. Besides complete history taking and physical examination
of the patients, B-scan sonography of lymphatic drainage areas and regional
lymph node regions was performed as part of the regular follow-up program
or for examination of clinical findings suggestive of lymphadenopathy detected
by the patients or the physician. In 20 examinations performed in 19 patients,
B-scan sonography revealed uncertain or suggestive results that qualified
for further investigation. One patient was investigated twice (in May and
August 2000) for different suggestive findings in B-scan sonography.
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Table 1. Characteristics of 19 Patients
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METHODS
Ultrasound examinations were performed by a single sonographer (M.-H.S.-W.)
using a real-time scanner (SSA-340 A; Toshiba Medical Systems, Neuss, Germany)
with an 8- to 10-MHz linear transducer. Lymphatic drainage areas and regional
lymphatic regions were examined and documented in horizontal and vertical
planes in every patient. Ultrasound assessment of detected lymph nodes was
first based on morphologic criteria, such as size, shape, and echogenicity
of the lymph node center and cortex. Solbiati Indices were calculated as the
ratio of maximal and minimal diameters in transversal and longitudinal sonographic
sections.7 Mainly following the recommendations
of Vassallo et al,8 lymph nodes were considered
metastatic if the following criteria were met: Solbiati Index less than 2
and/or predominance of low echogenicity of the whole lymph node structure
and/or lymph node center with low echogenicity and/or asymmetric regions with
low echogenicity in the lymph node margin. In all of the 20 B-scan ultrasound
examinations performed, melanoma metastases could not be excluded or verified
by clear sonomorphologic clues based on the criteria of Vassallo and colleagues.
For this reason, further diagnostic steps were considered necessary.
Initially, native color-coded sonography was performed to visualize
the vascularization of structures suggestive of lymphadenopathy. Velocity
and peripheral impedance of nodal vessels were examined by CDS, if possible.
Peak velocities were measured, and resistive indices (RIs)and pulsatility
indices (PIs) were determined according to Gosling and King9
and Pourcelot.10 The RI, representing the peripheral
vascular resistance, and the PI, representing the peripheral vascular obstruction,
were gained by an integrated function of the ultrasound device. The RI was
defined as the ratio of maximal systolic (Sm) minus end diastolic
(De) to maximal systolic (Sm) flow velocity:
The PI was defined as the ratio of maximal systolic (Sm)
minus end diastolic (De) to time-averaged maximum (Mav)
flow velocity:
Afterward, signal-enhanced CDS was performed by administration of an
ultrasound signal-enhancing agent (Levovist; Schering, Berlin, Germany), which
was applied intravenously as a bolus of 8 mL (concentration, 312.5 mg/mL).
The contrast agent suspension was prepared by adding sterile water to the
commercially available powder, which consisted of 99.9% D-galactose and 0.1%
palmitic acid. Fragmentation in microparticles and binding of small air bubbles
was induced by shaking the suspension. Intravenous application of the ultrasound
agent increased the scattering of ultrasound waves and led to a signal enhancement
up to 25 dB.11 Occurrence of first signal enhancement,
duration of signal enhancement, and possible adverse effects were documented.
As in native CDS, vascularization pattern and, if possible, RI and PI in CDS
were documented. Results of native and signal-enhanced CDS were compared,
and the value of quantitative variables, such as RI and PI for receipt of
additional differential diagnostic information was assessed.
According to Tschammler et al,12 different
intranodal vascular patterns contributed to reactive or malignant lymphadenopathy
as detected by native CDS. Patterns for reactive lymph nodes included hilar
or longitudinal vessels or branching of longitudinal vessels. Patterns for
metastases included accessory peripheral vessels, displacement of intranodal
vessels, asymmetric avascular areas, or aberrant course of central vessels.
In patients with structures highly suggestive of metastases and in uncertain
cases, excision and histopathologic examination were performed. In patients
with benign structures, follow-up examinations by sonography and/or computed
tomographic (CT) scanning were used to reconsider the diagnosis raised by
signal-enhanced CDS.
RESULTS
Morphologic criteria (size, shape, echogenicity) of the examined structures
in B-scan sonography are listed in Table
2. Administration of the D-galactose–based signal enhancer
was well tolerated by all 19 patients in 20 examinations. Neither pseudoallergic
reactions nor thermal sensations as described by Schlief et al11
could be observed in our patients.
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Table 2. Morphological Criteria of the Examined Structures by B-scan
Sonography
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In all patients, the signal enhancer was injected into a peripheral
hand or forearm vein as a bolus with an injection time of 5 to 10 seconds.
The first detectable effect could be perceived on average about 20 seconds
after injection, with a range of 5 to 30 seconds. Duration of signal-enhancing
effects was short (between 3 and 8 minutes).
Despite the short examination time, it was possible to document changes
in vascularity pattern after injection of the signal enhancer. In 14 (70%)
of 20 examinations, signal enhancement led to a better visualization of general
vessel topography, showing additional vessels after contrast enhancement or
enabling the investigator to describe the distribution of vessels in more
detail. In 11 examinations, vascularity could be detected only after application
of the contrast enhancer. In 3 examinations, vessel distribution could be
better described than in native CDS. In 6 examinations, application of signal
enhancer did not have any signal-enhancing effects. In 15 examinations, additional
information improving diagnostic certainty or influencing the therapeutic
concept could be achieved because of assessment of signal enhancement or lack
of signal enhancement after application of signal enhancer. In 3 examinations,
avascularity after administration of the signal enhancer did not help to distinguish
malignant from benign processes, and further diagnostic steps were initiated.
Excision and histopathologic examination revealed subcutaneous soft tissue
metastases in 2 patients and a superficially located lymph node metastasis
in 1 patient. Table 3 gives the
results in more detail.
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Table 3. Vascularization of Lesions Examined After Injection of Contrast
Enhancer and Evaluation of Additional Information
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However, because of the small diameter of blood vessels (0.1-0.3 mm)
in small lymph nodes, measurement of the RI and PI in CDS was not possible
in all examinations. In only 6 (30%) of 20 examinations could quantitative
variables be evaluated at all. The RI and PI could be determined in 2 examinations
before and after application of the signal enhancer, and in 4 examinations
quantitative variables could be determined only after application of the signal
enhancer. According to Tschammler et al,13
pathologic arterial Doppler spectra in metastatic lymph node vessels were
quantified with an RI of 0.9 or higher or a PI of 1.8 or higher. Before application
of the contrast enhancer, measurement of the PI and RI in native CDS did not
help to determine metastatic disease, which was found after histopathologic
examination after excision of the lesions. After application of the signal
enhancer, metastases tended to demonstrate higher PI values ( 1.8), correctly
indicating metastases in 3 patients. However, RI values did not exceed the
0.9 threshold, therefore leading to different results for the same lesions.
Metastases were assumed if CDS revealed perfusion primarily in peripheral
regions of structures suggestive of lymphadenopathy (Figure 1A-C) or in mixed pattern with hyperperfusion of one area
and lack of perfusion of another area. For structures highly suggestive of
lymphadenopathy after B-scan sonography and/or CDS, excision and histopathologic
examination were initiated. In 6 cases, histologic analysis confirmed the
preoperative diagnosis of metastases of malignant melanoma. In 1 patient,
a lymph node metastasis of thyroid cancer was found. In 2 patients, excision
of suggestive lesions disproved the assumption of melanoma metastases but
revealed the diagnosis of a reactive lymph node with marked vessel proliferation
in one patient and the diagnosis of a postoperative neuroma in the other.
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Figure 1. A melanoma metastasis in the patient's
left groin. A, B-scan sonography reveals an echo-poor roundish structure.
B, A lack of visible perfusion is found in native color Doppler sonography.
C, After application of the signal enhancer, a peripheral vascular pattern
can be demonstrated.
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In 2 patients, administration of signal enhancer led to visualization
of homogeneous color pixels in mainly echo-poor structures by application
of slight pressure with the transducer. Therefore, hematomas containing liquid
areas after prior lymph node dissection were assumed in 2 patients (Figure 2A and B). This was confirmed by histopathologic
examination in one patient and by sonographic control examinations with increase
of echogenicity during several weeks in the other.
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Figure 2. A hematoma at the patient's left
thigh. A, B-scan sonography reveals an indistinct echo-poor structure (transversal
scan). B, No vessels can be detected by native color Doppler sonography, but
homogeneous color pixels representing liquid areas can be detected in signal-enhanced
color Doppler sonography by application of slight pressure with the transducer.
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In 2 patients, echolucent, roundish structures without any signal enhancement
after injection of signal enhancer led to the presumptive diagnosis of postoperative
seromas that resulted from lymph node dissection. Sonographic-oriented fine-needle
aspiration revealed clear liquid in one patient who tested cytologically negative
for any malignant cells, confirming the diagnosis of a seroma. Sonographic
and CT follow-up examinations revealed identical findings consistent with
postoperative seroma throughout 6 weeks in the other patient.
A misdiagnosis of an atypical lipoma was established in 1 patient after
B-scan sonography revealed an indistinct, in part echo-rich, mainly echo-poor
structure (Figure 3).
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Figure 3. A melanoma metastasis misdiagnosed
as an atypical lipoma. B-scan sonography reveals an indistinct in part echo-rich
(arrow), mainly echo-poor structure (double arrows).
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The diagnosis of reactive lymph nodes was established after B-scan ultrasound
and signal-enhanced CDS for visualization of hilus vessels (sometimes with
branching to the lymph node margin) (Figure
4A-C) in 5 patients. In 1 patient, a small reactive lymph node was
assumed without any signal enhancement only because of B-scan ultrasound criteria.
All of these patients had at least 1 follow-up sonographic and/or CT scan
examination 4 to 8 weeks later. Since no signs of lymph node enlargement or
increase of echo-poor areas could be found during follow-up examinations,
the first diagnosis of reactive lymph nodes was confirmed in all 6 patients.
A synopsis of the results of contrast-enhanced CDS, postoperative histologic
analysis, cytologic analysis, and follow-up examinations is given in Table 4.
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Figure 4. A reactive cervical lymph node.
A, B-scan sonography reveals a global echo-poor structure with an asymmetric
echo-poor area in the lymph node periphery in the sagittal scan. B, Some rare
vessels but no vascular pattern can be detected by native color Doppler sonography.
C, After application of the signal enhancer, a hilus vessel with branching
to the lymph node periphery can be detected by color Doppler sonography.
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Table 4. Synopsis of Results of Signal-Enhanced Color Doppler Sonography,
Histologic Analysis, Cytologic Analysis, and Follow-up Examinations*
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COMMENT
Administration of ultrasound contrast enhancers has been shown to be
helpful in echocardiography for diagnosis of left heart failure and for the
examination of vessels such as the transcranial arteries, renal arteries,
or portal veins.14-16
In all of these indications, the amplitude of ultrasound signals is increased
after application of a signal enhancer. In the case of the D-galactose–based
contrast enhancer Levovist, shaking of the contrast suspension leads to fragmentation
in microparticles and binding on small air bubbles. This induces an increase
of scattering and, therefore, a signal enhancement, which can be used for
diagnosis of intravascular blood flow even in very small vessels (0.1-0.3
mm in diameter).17
Recently, intravenous application of Levovist was reported to improve
visualization of vessel topography in lymph nodes of patients with squamous
cell carcinomas of the head and neck and in lymph nodes of patients with malignant
Hodgkin and non-Hodgkin lymphomas.18-19
The authors found signal-enhanced CDS superior to native CDS in the differentiation
of malignant from reactive lymph nodes of the neck.
To our knowledge, the current prospective study reports for the first
time the results of lymph node ultrasound examinations using the D-galactose–based
contrast enhancer in patients who present with structures suggestive of lymphadenopathy
in B-scan ultrasound during follow-up for cutaneous melanoma. In 15 of 20
examinations, correct additional information improving diagnostic certainty
could be obtained because of signal enhancement or lack of signal enhancement
after application of signal enhancer. Two hematomas and 2 seromas could be
diagnosed correctly. Five of 7 reactive lymph nodes showed hilus vessels,
in part with branching to the lymph node periphery, and 1 small reactive lymph
node remained avascular. Both flow patterns are described for reactive lymph
nodes. Five of the 8 histologically proven metastases revealed a peripheral
flow pattern or a mixed pattern with avascular areas and areas with a chaotic
intranodal flow. These vascular patterns are in accordance with those described
by Tschammler et al,12 who investigated reactive
and malignant lymph nodes in patients with varying tumors using color Doppler
flow imaging but no signal enhancer. However, in our study, 1 histologically
proven lymph node metastasis and 2 soft tissue metastases did not reveal any
vascularity after application of the contrast enhancer. A similar effect was
reported by Moehrle et al,6 who investigated
melanoma patients using native CDS. They found the absence of vessels or a
reduced perfusion to support the diagnosis of melanoma metastases. Moehrle
and colleagues speculated that avascular regions may represent necrotic areas
within metastatic lymph nodes. In our patients, all avascular metastases (1
lymph node metastasis, 2 soft tissue metastases) were located rather superficially
within the subcutaneous tissue. A possible explanation for the avascularity
of superficially located metastases may be the short-lasting contrast-enhancing
effect, which may end before those metastases can be visualized.
In addition to qualitative variables such as nodal morphological structure
and distribution of vascularity, quantitative variables such as velocity and
corresponding RI and PI have been investigated to obtain more objective criteria.
In the past, different groups tried to establish quantitative thresholds for
defining vascularity of malignant respectively benign lymph nodes.13, 20-22 Choi
et al21 defined a PI more than 1.5 and an RI
more than 1.0 to be characteristic for malignancy, whereas Steinkamp et al22 postulated 1.6 and 0.8 as thresholds for PI and RI,
respectively. The most often used classification is the one of Tschammler
et al,13 who found lymph nodes with a PI of
1.8 or more and an RI of 0.9 or more to be suggestive of malignancy. In our
patients, quantitative variables were disappointing. In only 2 of 20 examinations,
the RI and PI could be determined before application of the signal enhancer.
In both examinations, the RI and PI did not reveal pathologic values and therefore
did not help support the diagnosis of metastases, which were suspected on
morphologic criteria and subsequently confirmed by histopathologic analysis.
In 6 of 20 examinations, measurement of quantitative variables after application
of the contrast enhancer was possible, yet in only 3 of 8 metastases did PIs
exceed the 1.8 threshold, correctly indicating malignancy. The RIs did not
exceed the 0.9 threshold in these examinations. Our results are in accordance
with those of other investigators who recently were unable to confirm former
data on PI and RI thresholds differentiating malignant from benign lymph nodes
without application of a signal enhancer.12, 23-24
Moehrle et al6 speculated that melanoma metastases,
investigated by native CDS, may have lower indices than metastases of other
malignancies. However, in our study, indices could be increased after application
of the signal enhancer in 3 of 8 metastases, indicating that melanoma metastases
do not generally have lower vascularization indices than metastases of other
tumors. Although some of the metastases tended to demonstrate higher PIs exceeding
1.8 in our patients, qualitative variables do not allow a reliable differential
diagnosis, since measurements were possible in only 6 of 20 examinations.
Recording of Doppler spectra and calculation of RI or PI seem to be time-consuming
and of little diagnostic value in this context.
In conclusion, administration of the D-galactose–based contrast
enhancer gave additional information on sonomorphologic aspects of vascularity
for differentiation of reactive lymph nodes, lymph node metastases, hematomas,
and seromas. Yet, for soft tissue metastases or superficially located small
lymph node metastases, D-galactose–based CDS was not clearly superior
to native CDS. Improved accuracy of diagnosis was mainly because of qualitative
assessment of vascularity. Quantitative variables such as PI and RI were not
of high diagnostic value. However, further prospective studies in larger patient
groups might be helpful to evaluate the possible beneficial effect of ultrasound
signal enhancers for differentiating malignant from reactive lymph nodes in
patients with cutaneous melanomas in more detail.
AUTHOR INFORMATION
Accepted for publication May 21, 2001.
Corresponding author and reprints: Monika-Hildegard Schmid-Wendtner,
MD, Department of Dermatology and Allergology, Ludwig-Maximilians-University,
Frauenlobstr 9-11, D-80337 Munich, Germany (e-mail: M.Schmid-Wendtner{at}LRZ.uni-muenchen.de).
From the Department of Dermatology and Allergology, Ludwig-Maximilians-University,
Munich, Germany.
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