Evaluation of vascular patterns of cervical lymph nodes with power Doppler sonography

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Evaluation of Vascular Patterns of Cervical Lymph Nodes with Power Doppler Sonography Francesco Giovagnorio, MD, Rossella Caiazzo, MD, and Alessandra Avitto, MD Abstract: Power Doppler sonography was used to evaluate 105 benign and malignant cervical lymph nodes in 60 patients. Three main vascular patterns were identified: type I (single vascular pole), type II (hypertrophic vascular pole), and type III (mainly pe- ripheral vascularity). The first one was related to chronic inflammation (sensitivity 85%, specificity 90%); the second and third were related, to a lesser extent, to acute inflammation and neoplasm (sensitivity 68% and 55%, specificity 47% and 91%, respec- tively). The authors conclude that the sensitivity and specificity of power Doppler so- nography cannot compete with those of fine-needle aspiration biopsy in the diagnosis of adenopathy. © 1997 John Wiley & Sons, Inc. Indexing Words: Lymphatic system z Lymph node neoplasms z Color Doppler z Doppler ultrasonography Diagnostic imaging has always played an impor- tant role in the evaluation of lymph nodes, but, despite the impressive technical progress, a de- finitive diagnosis still requires an invasive ap- proach such as surgical excision or aspiration bi- opsy. The use of ultrasound however, has proven effective in detecting nodes and in analyzing some morphologic features that are frequently associ- ated with malignancy, such as roundness, 1 ab- sence of echogenic hilum, 2 and presence of central tubular structures representing small arteries encased in neoplastic tissue. 3 The introduction of color Doppler sonography (CD) has multiplied the amount of information that can be obtained during an ultrasound exami- nation, because since this technique can easily collect interesting data about the vascularity of parenchymatous structures, the application of CD to lymph node analysis, however, has not demon- strated a definite clinical usefulness. 4–9 Power Doppler sonography (PD), a interesting evolution of the color Doppler technology, seems even more promising in the detection of low flow in small structures: PD calculates the integrated power of the Doppler signal instead of the mean frequency, so it does not alias, is angle-independent, and is not substantially affected by noise. 10–12 To date, no applications of PD in the evaluation of adenop- athy have been reported, but the ability of PD to detect low flow could give this technique a sub- stantial advantage over CD. The aim of this study was to evaluate the po- tential superiority of power Doppler sonography over color Doppler sonography in finding typical vascular patterns which could be of help in differ- entiating between benign and malignant adenop- athy. MATERIALS AND METHODS We studied 60 patients with one or more palpable superficial cervical nodes (105 lymph nodes) clini- cally divided into three categories: (1) probable acute adenitis (signs of acute inflammation in an anatomical site and painful nodes in a satellite location); this group included 12 patients with 16 nodes; (2) ‘‘risky’’ nodes (asymptomatic patients From the Sezione di Radiologia e Diagnostica per Immagini, Dipartimento di Medicina Sperimentale e Patologia, Univer- sita ` ‘‘La Sapienza,’’ Viale Regina Elena, 324, 00161 Rome, Italy. For reprint requests contact Dr. Francesco Giovagnorio at present address: I Cattedra di Radiologia, Policlinico Um- berto I, Viale Regina Elena, 324, 00161 Rome (Italy); e-mail [email protected]. J Clin Ultrasound 25:71–76, February 1997 © 1997 by John Wiley & Sons, Inc. CCC 0091-2751/97/020071-05 71 VOL. 25, NO. 2, FEBRUARY 1997

Transcript of Evaluation of vascular patterns of cervical lymph nodes with power Doppler sonography

Evaluation of Vascular Patterns of CervicalLymph Nodes with Power

Doppler Sonography

Francesco Giovagnorio, MD, Rossella Caiazzo, MD, andAlessandra Avitto, MD

Abstract: Power Doppler sonography was used to evaluate 105 benign and malignantcervical lymph nodes in 60 patients. Three main vascular patterns were identified: typeI (single vascular pole), type II (hypertrophic vascular pole), and type III (mainly pe-ripheral vascularity). The first one was related to chronic inflammation (sensitivity85%, specificity 90%); the second and third were related, to a lesser extent, to acuteinflammation and neoplasm (sensitivity 68% and 55%, specificity 47% and 91%, respec-tively). The authors conclude that the sensitivity and specificity of power Doppler so-nography cannot compete with those of fine-needle aspiration biopsy in the diagnosis ofadenopathy. © 1997 John Wiley & Sons, Inc.Indexing Words: Lymphatic system z Lymph node neoplasms z ColorDoppler z Doppler ultrasonography

Diagnostic imaging has always played an impor-tant role in the evaluation of lymph nodes, but,despite the impressive technical progress, a de-finitive diagnosis still requires an invasive ap-proach such as surgical excision or aspiration bi-opsy. The use of ultrasound however, has proveneffective in detecting nodes and in analyzing somemorphologic features that are frequently associ-ated with malignancy, such as roundness,1 ab-sence of echogenic hilum,2 and presence of centraltubular structures representing small arteriesencased in neoplastic tissue.3

The introduction of color Doppler sonography(CD) has multiplied the amount of informationthat can be obtained during an ultrasound exami-nation, because since this technique can easilycollect interesting data about the vascularity ofparenchymatous structures, the application of CDto lymph node analysis, however, has not demon-

strated a definite clinical usefulness.4–9 PowerDoppler sonography (PD), a interesting evolutionof the color Doppler technology, seems even morepromising in the detection of low flow in smallstructures: PD calculates the integrated power ofthe Doppler signal instead of the mean frequency,so it does not alias, is angle-independent, and isnot substantially affected by noise.10–12 To date,no applications of PD in the evaluation of adenop-athy have been reported, but the ability of PD todetect low flow could give this technique a sub-stantial advantage over CD.The aim of this study was to evaluate the po-

tential superiority of power Doppler sonographyover color Doppler sonography in finding typicalvascular patterns which could be of help in differ-entiating between benign and malignant adenop-athy.

MATERIALS AND METHODS

We studied 60 patients with one or more palpablesuperficial cervical nodes (105 lymph nodes) clini-cally divided into three categories: (1) probableacute adenitis (signs of acute inflammation in ananatomical site and painful nodes in a satellitelocation); this group included 12 patients with 16nodes; (2) ‘‘risky’’ nodes (asymptomatic patients

From the Sezione di Radiologia e Diagnostica per Immagini,Dipartimento di Medicina Sperimentale e Patologia, Univer-sita ‘‘La Sapienza,’’ Viale Regina Elena, 324, 00161 Rome,Italy. For reprint requests contact Dr. Francesco Giovagnorioat present address: I Cattedra di Radiologia, Policlinico Um-berto I, Viale Regina Elena, 324, 00161 Rome (Italy); [email protected].

J Clin Ultrasound 25:71–76, February 1997© 1997 by John Wiley & Sons, Inc. CCC 0091-2751/97/020071-05

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with one or more non-painful nodes or patientswith an already diagnosed malignancy in the T1–T2 stage with nodes in satellite or non-satellitelocations); this group included 43 patients with 83nodes; (3) ‘‘end-stage’’ nodes (patients with an al-ready diagnosed malignancy in the T3–T4 stagewith 3 or more >2 cm nodes in a satellite location);this group included 5 patients with 6 nodes.Antibiotic therapy was administered to groups

1 and 2: the patients who did not show any posi-tive evolution of their adenopathy (significant re-duction) after 10 days of therapy underwent his-tological examination, which was performed in 4nodes of group 1 and in all 83 nodes of group 2 (70of whom underwent fine-needle aspiration biopsyand 13 were surgically excised); biopsy was notperformed in the 6 nodes of group 3.The Doppler examinations, performed before

biopsy or therapy, were carried out with 10-MHzlinear transducers (SPECTRA VST, Diasonics,Milpitas, CA, and IDEA, Esaote Biomedica, Ge-noa, Italy) in longitudinal and axial scans; weused a PRF of 750 Hz (Idea) and 700 Hz (SpectraVST), with a color window enclosing the entirefield of view. To reduce transmitted motion frompulsating vessels, we used the so-called ‘‘motionfilter’’ (which acts as a high-pass filter) on theSpectra VST and the corresponding ‘‘wall filter’’on the Idea. As suggested by Bude and co-workers,10 color gain was manipulated until‘‘color noise’’ became apparent in the image back-ground (for CD examination) and until it first be-gan to exceed the homogeneous single-color back-ground of the window (for PD examination). Theresulting settings were subsequently applied toall the nodes examined. The cine-review modewas used to freeze images in peak-systolic phase,for a better depiction of arterial flow.Based on the CD and/or PD evidence, we clas-

sified the vascular patterns of the nodes intothree types (Figure 1).● Type I: a single vascular pole in the hilum witha small artery entering the node (Figure 2).

● Type II: hypertrophic single vascular pole withthe main hilar feeding artery almost doubled indiameter and length (as compared to type I),and two or more branching arteries in the cen-ter of the node (Figure 3).

● Type III: mainly peripheral vascularity withthree or more vascular branches perforatingthe capsule peripherally and directed towardthe center of the node (Figures 4 and 5).

RESULTS

Histological and clinical evaluation classified the105 nodes into acute inflammatory adenopathy(16 nodes, or 15%), chronic inflammatory or reac-tive adenopathy (42 nodes, or 40%) and lymphnode metastasis (47 nodes, or 45%); histologicalanalysis of metastatic nodes demonstrated metas-tasis from carcinoma of the oral cavity (7 nodes),larynx (6 nodes), breast (4 nodes), thyroid (9nodes), lung (7 nodes); 9 nodes showed lymphomaand 5 remained of unknown origin. The clinicaland pathological classification of the nodes is pre-sented in Table 1.A relevant fraction of the nodes (76%) showed

signs of vascularity with CD, whereas PD de-tected one or more vascular poles in 100% ofthem. Although as noticed by Bude,10 the com-parison is obviously subjective and cannot be ad-equately quantified, in no case did we doubt theobvious superiority of the power Doppler sono-grams.A total of 47 nodes (45%) were classified into

type I (single vascular pole); 40 were chronic in-flammation and while 7 were neoplastic. Type II

FIGURE 1. The three vascular patterns observed: type I (single vascular pole in the hilum, with a small artery entering the node); type II

(hypertrophic single vascular pole, with the main hilar feeding artery almost doubled in diameter and length and two or more branching arteries

in the center of the node); type III (mainly peripheral vascularity, with three or more vascular branches perforating the capsule peripherally and

directed toward the center of the node).

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(hypertrophic vascular pole) comprised 27 nodes(25%), 11 with acute inflammation, 2 with chronicinflammation, and 14 with metastasis. The last31 nodes (30%) were classified into type III (pe-ripheral vascularity), divided into 5 acute inflam-matory and 26 neoplastic nodes.Sensitivity (SE), specificity (SP), and positive

and negative predictive values (PPV and NPV)were calculated for each of the three classes ofvascularity with the three histological/clinicalclasses: as the most relevant values, the associa-tion of type I (single vascular pole) with chronicinflammation showed a SE of 85%, a SP of 90%, aPPV of 85%, and a NPV of 96%. The association oftype II (hypertrophic vascular pole) with acuteinflammation showed a SE of 68%, of SP of 47%,a PPV of 0% and a NPV of 72%. The association oftype III (peripheral vascularity) with metastasisshowed a SE of 55%, a SP of 91%, a PPV of 83%and a NPV of 71%. The complete distribution ofstatistical values is given in Table 2.

FIGURE 2. Submandibular, 1.2 cm wide, non-painful node in a 47-

year-old patient with no relevant clinical symptoms: power Doppler

sonography demonstrates a small vascular pole (vascular pattern

type I). Biopsy: signs of chronic, non-specific inflammation.

FIGURE 3. Submental, 2-cm wide, painful node in a 22-year-old pa-

tient with herpetic dematitis of the lower lip: power Doppler sonog-

raphy demonstrates hypertrophic hilar vessels (vascular pattern type

II). Diagnosis following clinical remission: acute adenitis.

FIGURE 4. Right laterocervical, 1-cm wide, non-painful node in a 57-

year-old patient with a papillary carcinoma in the right lobe of the

thyroid. Power Doppler sonography demonstrates a mainly periph-

eral vascularity (vascular pattern type III). Biopsy: metastasis from

papillary carcinoma.

FIGURE 5. Lower left laterocervical, 2.5-cm wide, non-painful node in

a 45-year-old patient with no relevant clinical symptoms. Power

Doppler sonography demonstrates intense peripheral vascularity

(vascular pattern type III). Biopsy: metastasis from melanoma of un-

known origin.

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DISCUSSION

Sonographic evaluation of lymph nodes has al-ways been a difficult task because of the technicallimitations of the method and the complicated pa-thology of the nodes. Although the progressivelyincreasing spatial resolution of ultrasound im-ages permits a deeper examination of the struc-tural features of the node, the low sensitivity andspecificity of ultrasound cannot be compared withthose of fine-needle aspiration biopsy, which pro-vides accurate information about the eventful ma-lignancy along with the histologic characteristicsof the neoplasm at the expense of limited invasiv-ity. Moreover, the pathology of lymph nodes doesnot help the sonograph because the alterations ofthe normal structure are complex and sometimesunpredictable. For example, it is impossible to de-fine the architecture of a ‘‘normal’’ node becausein normal adults, a lymph node that never under-went reactive changes can hardly be found. Onthe other hand, inflammatory changes can be sowidespread as to mimic a neoplastic colonization,whereas micrometastases usually preserve thearchitecture of the node.14

The introduction of color Doppler sonographyhas increased the amount of data that can be col-lected during the ultrasound examination of anode, but it is now clear that vascular changeswhich take place in an abnormal node are even

more unpredictable than simple morphologicalchanges. An increased vascularity with lower im-pedance, for example, can be found during acuteinflammation, because edema and vasodilatationcause a substantial increase of flow in the capil-lary network. Unfortunately, a reactive prolifera-tion of blood vessels can also be seen in anychronic non-specific reactive lymphadenopathy,while neoplastic infiltration is followed by an ac-tive angiogenesis, probably due to the productionof tumor angiogenetic factor (TAF) by the tumorcells.14–16 On the other hand, a decreased vascu-larity with high impedance can express the vas-cular compression of small arteries that occursduring intense acute inflammation, the fibroticchanges of a chronic inflammation, or vascularinfiltration or encasement by neoplastic tissue.16

For these reasons, reports on the Doppler ultra-sound evaluation of lymph nodes has not pro-duced comparable nor standardizable results: in-creased vascularity or changes in resistive indexcannot be proposed as reliable parameters.4–9

Recently, a new method to collect and displaydata derived from Doppler sonography has beendeveloped: the name ‘‘power Doppler,’’ used by themajority of manufacturers, reflects the parameterthat the method is focused on.10–13 Although con-ventional color Doppler sonography is based onmean frequency (because this parameter is calcu-

TABLE 2

Distribution of Vascular Patterns

Acute inflammation Chronic adenopathy Metastases

Type I 0 nodes 40 nodes 7 nodes

(single vascular pole) SE 00% SP 47% SE 85% SP 90% SE 14% SP 31%

PPV 00% NPV 72% PPV 85% NPV 96% PPV 14% NPV 31%

Type II 11 nodes 2 nodes 14 nodes

(hypertrophic pole) SE 68% SP 82% SE 05% SP 61% SE 29% SP 77%

PPV 40% NPV 93% PPV 07% NPV 51% PPV 51% NPV 57%

Type III 5 nodes 0 nodes 26 nodes

(peripheral vascularity) SE 31% SP 70% SE 00% SP 50% SE 55% SP 91%

PPV 16% NPV 85% PPV 00% NPV 43% PPV 83% NPV 71%

SE = sensitivity; SP = specificity; PPV = positive predictive value; NPV = negative predictive value.

TABLE 1

Clinical and Histologic Classification of Nodes

Histologicclassification

Probable acuteinflammation

’’Risky’’nodes

Neoplasticnodes Clinical FNAB Excision Total

Acute inflammation 16 0 0 12 4 0 16 (15%)

Chronic adenopathy 0 42 0 0 37 5 42 (40%)

Metastasis 0 41 6 6 33 8 47 (45%)

Total 16 83 6 18 74 13

(15%) (79%) (6%) (17%) (70%) (13%)

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lated when assigning color hue to each pixel),with power Doppler sonography the parameter onwhich the color scale is calculated is the ‘‘power’’or ‘‘intensity’’ of the signal, which expresses indi-rectly the number of red blood cells insonated bythe ultrasound beam. Power Doppler sonographyis less dependent on Doppler angle than is meanfrequency color Doppler and is, therefore, less af-fected by aliasing because changes of the in-sonation angle and PRF does not affect the num-ber of red cells insonated by the ultrasound beam.Furthermore, power Doppler sonography pro-duces a substantial cut-off in background noise,thus increasing low-flow sensitivity: in fact, again increase of 10 dB–15 dB has been reported.11

The major drawback of power Doppler sonogra-phy is that the entire color scale is used to expressflow intensity, so that no differentiation in flowdirection can be obtained. This factor limits theexamination to those cases requiring only anevaluation of global flow.We decided to use the high sensitivity of power

Doppler sonography to attempt to qualitativeanalysis of vasculature of lymph nodes; close ob-servation suggested the subdivision into threetypes, which seem to follow closely the pathologi-cal changes in nodal vasculature. Type I (singlevascular pole in the hilum, with a small arteryentering the node) should be observed in nodeswith no significant changes. Type II (hypertrophicsingle vascular pole, with the main hilar feedingartery almost doubled in diameter and length andtwo or more branching arteries in the center ofthe node) should express a substantial, but stillregular, increase in blood flow. Type III (mainlyperipheral vascularity, with three or more vascu-lar branches perforating the capsule peripherallyand directed toward the center of the node) shouldindicate an exuberant and chaotic hypervascular-ity, expressed by hyperemic changes of the perfo-rating arteries, which become necessary to assurethe increase in blood flow that the disease re-quests.Our initial observations seemed to point to a

possible correlation between chronic inflamma-tion and type I, acute inflammation and type II,metastasis and type III. Later observations andstatistical analysis, however, confirmed the firstobservation (SE 85% SP 90%) but did not producesubstantial evidence for the second and third (SE68% SP 47%, SE 55% SP 91%, respectively). Thisexperience confirms the assumption that in-creased vascularity reflects acute disease, but theassociations between vascular patterns and dis-eases are so complex and unpredictable that theyescape the sensitivity of Doppler ultrasound scan-

ners. However, the close correlation between typeI and acute adenitis, and the high specificity oftype III in cases of metastases might suggest thataspiration biopsy can be excluded when the rightvascular pattern is associated with the appropri-ate clinical signs.The low sensitivity of type III in cases of me-

tastases is due to the frequent destruction ofnodal architecture caused by neoplastic cells. Insuch cases, the newborn vascular net is infil-trated and, therefore, invisible, so that a ‘‘pseudo-type I’’ is detected. However, a close analysis ofthe morphology of the node is generally sufficientto avoid misdiagnosis.In conclusion, power Doppler sonography is su-

perior to color Doppler sonography in the assess-ment of nodal vascularity. The sensitivity andspecificity of power Doppler parameters cannotcompete yet with those of fine-needle aspirationbiopsy, which remains ‘‘gold standard’’ in the di-agnosis of lymph node disease, but an associationbetween definite patterns of flow and a specificcause of disease seems evident. It is possible thatpower Doppler sonography will find a role in thefollow-up of adenopathy (where it could be usefulin detecting post-therapeutic changes in vascular-ity) or as a guide to biopsy, which could be per-formed only on the members of a group that canbe differentiated from the others on the basis ofparticular signs.

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