Ruben

Kier,

Renal with

MD

#{149} Kenneth

Masses: Doppler

J. W. Taylor,

terms:

Angiomyolipoma,

91.3141

hemorrhage, 91.413 #{149} Kidney, infection, 91.212 #{149} Kidney neoptasms, US studies, 81.12984 #{149} Ultrasound (US), Doppler studies, 81.12984 Kidney,

cysts,

Radiology

91.31

1990;

Kidney,

#{149}

176:703-707

LTHOUGH

From the Department of Diagnostic Radiology, Yale University School of Medicine, 333 Cedar St, P0 Box 3333, New Haven, CT 06510. From the 1989 RSNA scientific assembly. Received January 10, 1990; revision requested March 8; final revision received May 10; accepted May 1 1 . Supported by American Cancer Society grant PDT 936 and National Institutes of Health grant ROl CA41729-01 Al. Address C

requests

RSNA,

1990

to R.K.

#{149} Ann

computed

(CT) and bowed improved renal

mass

have

addressed

L Feyock,

RT, RDMS

that

raise

such tions,

tomography

sonography detection

lesions

(1-3),

the

few

(4). Many imaging

concern

cyst

articles

of nerenal findings

for malignancy,

as septations, small or high attenuation

Although

have a!of small

specificity

nal mass detection cystic lesions have

calcificaat CT

puncture

and

(5).

opacifi-

cation was occasionally performed, most of these patients are followed up with serial imaging. Fine-needle aspiration of renal mass lesions unden sonographic or CT guidance has

been

disappointing,

with

ity of only 20%-62% thusiasm about the

renal nance

a sensitiv-

(2). Despite encapability to stage

neoplasms with magnetic reso(MR) imaging (6), MR imaging

has proved to be relatively limited in the detection and characterization of renal masses (7,8). Doppler ultrasound (US) has shown high sensitivity in the detection of tumor vasculanity within a variety of malignant lesions involving the liver, kidneys, adrenal gland, and

pancreas shown quencies carcinomas spectively nal mass established

(9,10). abnormal

Two studies have Doppler shift fre-

in 78%-83% of renal cell (1 1,12). This report proanalyzes indeterminate nelesions with use of criteria during one of those earli-

en retrospective

studies

MATERIALS

AND

During through nal mass

reprint

PhD

#{149} Isabel

M. Ramos,

MD

Characterization US’

The vascularity of indeterminate renal masses in 70 patients was investigated prospectively with duplex ultrasound. The peak-systolic Doppler shift frequency obtained from the renal mass was utilized to attempt distinction between benign and malignant lesions. With use of the criterion of a peak-systolic Doppler shift frequency of 2.5 kHz or greater as evidence of neovascularity, 26 of 37 malignant lesions demonstrated tumor signals (70% sensitivity). Thirty-one of 33 benign lesions lacked tumor signals (94% specificity). Both of the false-positive lesions were infections with inflammatory masses, with peak frequencies of 3.0 and 3.7 kHz. Tumor vascularity in most malignant renal mass lesions gives rise to abnormal, high-frequency, Doppler-shifted signals that can aid the differential diagnosis of renal masses. Index

MD,

basis

studies

of

tially with sonography (18 masses), or excretory masses). For 36 masses, nosis was subsequently either surgery the diagnosis

(42 masses), CT urography (10 a histologic diagmade by means

or biopsy. For was established

(a) definitive simple cyst

correlative at follow-up

phy, fat at CT [angiomyolipoma], mal parenchymal enhancement [ prominent lobation, columns

tion

of inflammatory lesions),

or (c) clinical

equipment

(Mark

vanced Wash)

was

ating ten

600

Technology used

in all

frequency was

Hz).

set

was

as low

Sample

volume

mass,

shift the

UltraMark

8; Ad-

The

wall

(50

or

volume

was

astolic frequencies were the Pourcelot index was

recorded, calculated.

the artery

US

and

ipsilateral the

corded.

was

or

size

METHODS

tumor tively

signals were as malignant probability

and In 24 main

Doppler

reTumor

frequency

shift frequencies (11). Renal masses

The

defined

to

Doppler and end-di-

with

was

a

the

contralateral

assessed

peak-systolic

Lesion

Once

reduced

the

renal

at 10

around

5 or 3 mm to better define shift frequency. Peak-systolic

cases,

fil100

manipulated of the mass.

detected

sample

inson-

The

was set initially was

was

Bothell,

studies. 3 MHz.

as possible

mm, and the cursor around the periphery

Doppler

or

Laboratories,

were

patients.

fol-

low-up for a minimum of 13 months. Commercially available duplex US

Doppler greater

105

a minienresolu-

or stability

lesions,

benign

signals

Doppler sonography of these masses was used prospectively to attempt their categonization as either benign or malignant, with use of criteria established in a prior retrospective series of 49 patients (1 1). Masses that were diagnosed confidently as benign (eg, simple cyst) on initial imaging studies were not referred for Dopplen sonognaphy.

or norat CT of Bertin,

and scar]), (b) serial imaging for mum of 5 months (eg, progressive largement of malignant lesions, of other

of

34 masses, by either

imaging (eg, CT or sonogra-

(1 1).

the period from October 1987 January 1990, indeterminate relesions were diagnosed on the

of imaging

Seventy renal masses with an established diagnosis constitute the study population. These lesions were imaged mi-

measured.

as peak-systolic

of 2.5 kHz demonstrating

diagnosed lesions.

or

prospec-

of malignancy

based

on

imaging findings alone was assessed retrospectively. The probability was considered high for solid or complex masses measuring

6 cm

or larger

and

low

for

masses 3 cm on smaller that were either (a) isoattenuated or isoechoic to normal renal parenchyma on the original imaging study remaining

or (b) predominately renal masses were

cystic. assigned

termediate probability. These retrospective assignments were then correlated with Doppler data and final diagnosis

The in-

to

703

KHz P

E A K

8

S

*

rO.O9

*

14

N U M B E

-

10

12

R

V

BENIGN

MALIGNANT

10

0

S

F

T

0

R

E N

Ii C

I:

F R

E Q U E

:

N

C V

0

**

MALIGNANT

LESION

DIAMETER

A

L M A

S S E S

#{176}

0

O11

(CM)

PEAK

1.

2.5-4

SYSTOLIC

DOPPLER

4.1-6

SHIFT

6.1-8

(KHz)

2.

Figures

1, 2.

relation

coefficient

(1) Correlation

of the

equaled

.09,

size

of malignant

indicating

renal

no correlation.

lesions

with

peak-systolic

(2) Distribution

Doppler

of peak-systolic

shift

frequency

frequency shifts

obtained for

benign

from and

the

lesion.

malignant

Cormasses.

Il

S T

0

0

L

0 G

*

$ARC

0

METS

5

MISC

0

WILM

x

V

ol

2.5

0

5

PEAK

Figure

3.

shift

DOPPLER

Malignant

according tnibuted

7.5

SYSTOLIC

renal

SHIFT

lesions

to 1KHz)

divided

to histologic diagnosis according to peak-systolic

and disDoppler

frequency.

TCCA transitional-cell SARC = sarcoma, METS metastases to the kidney, MISC miscellaneous malignancy, WILM = Wilms tumor, RCCA renal cell carcinoma.

carcinoma,

assess

the

in each The

relative

of those study

was

Investigation

utility

three

of Doppler

US

groups.

approved

Committee

by

the

of Yale

Human Univer-

sity, and verbal consent was obtained from the patient or a family member. The spatial peak/average intensity was reduced

with

the

equipment

attenuator

by

-9 dB to approximately 120 mW/cm2 with further tissue attenuation reducing this

to less

than

40

mW/cm2

at the

tumor

benign

Mean

systolic

frequency

artery

was .

the Pourcebot inratio of the peak-

significantly

Radiology

to the

masses

Figure

Thirty-seven renal masses were malignant and 33 masses were benign. The Doppler data are summanized in Table 1 . Peak-systolic frequency shift was significantly different between benign lesions (mean, 0.9 kHz) and malignant lesions (mean, 3.6 kHz). End-diastolic frequency shift was also significantly

although not. The

size

are

was

did

the peak-systolic (Fig 1).

RESULTS

different, dex was

and

data

main

different

renal

be-

malignant

tion

from

not

± 3.6 for maof malignant

correlate

with

frequency

2 demonstrates malignant

only

3.4 cm ± 2.0 for be-

of peak-systolic

among

lesions,

available

nign lesions and 6.6 cm lignant lesions. The size

renal

site.

704

tween although 24 cases.

shift

the

distnibu-

formed

masses. Whereas the majority of malignant lesions (26 of 37) had a peaksystolic frequency shift of 2.5 kHz or greater (70% sensitivity), only two of the 33 benign lesions had a shift in this range (94% specificity). Figure 3

separates shift

the

peak-systolic

of malignant

to their histologic teen of 24 renal had

peak-systolic

lesions

cell

frequency according

diagnosis. carcinomas

Doppler

kidney

known where ment

benign

Eigh(75%)

shifts

of

4-7).

All four peak of 2.5 kHz or

greater. All three cases of transitional cell carcinoma demonstrated low frequency shifts. The misceblaneous category refers to large mass lesions in the

frequency

versus

2.5 kHz or greater (Figs Wilms tumors demonstrated systolic frequency shifts

in patients

who

primary malignancy but in whom histologic of the

kidney

was

to determine

according

per-

the

tumor

ne-

or a

lesions

to their

a

elseassess-

whether

nal mass was a primary metastasis to the kidney. The 33 benign renal

classified

not

had

are

diagnos-

tic categories in Figure 8. Only two benign renal masses demonstrated peak-systolic frequency shifts over 2.5 kHz. These exceptions occurred in two of eight cases of renal infection that demonstrated frequency shifts of 3.0 and 3.7 kHz. Both pa-

September

1990

a.

b.

Figure

4.

Renal

cell

carcinoma

C.

in a patient

with

chronic

renal

failure

undergoing

peritoneal

dialysis.

(a) CT scan

demonstrates

a complex

cystic mass in the left kidney (arrow). Adjacent images demonstrated simple cysts in both atrophic native kidneys. Free fluid in the left pencolic gutter is from penitoneal dialysis. (b) Sonogram of the left kidney demonstrates a complex cystic mass. The Doppler cursor was manipulated around the periphery of this mass to obtain Doppler signals. (c) Doppler spectrum of the left renal mass demonstrates peak-systolic frequency of almost 6 kHz, consistent with malignancy.

b.

a. Figure

5.

Renal

cell

carcinoma

C.

manifesting as hematuria. is slightly hyperattenuated

the left kidney (arrow) that mass to be slightly hypoechoic. The Doppler peak-systolic frequency of 4 kHz, consistent

(a) CT scan obtained with respect to normal

cursor is at the periphery with malignancy.

83%

assigned an intermediate probability, with malignancy diagnosed in 12 (28%). Table 2 assesses the utility of

cy shifts

of 2.5

hypovasculan Volume

kHz

or greater.

or avasculan 176

#{149} Number

3

Of

masses

11

carcinoma,

(c) Doppler

(five

Seventeen masses (14 malignant, three benign) were assessed with angiography. Of six masses (all renal cell carcinoma) that were hypervascular or vascular at angiography, five demonstrated peak-systolic frequen-

cell

of the mass.

tients demonstrated clinical evidence of infection. Among patients in whom the main renal artery was sampled, the renal mass frequency shift exceeded that of the artery for 1 1 of 12 malignant lesions and two of 12 benign lesions (92% sensitivity, 83% specificity, 87% accuracy). In this same group, a peaksystolic frequency cutoff of 2.5 kHz was 75% sensitive, 92% specific, and accurate.

renal

without intravenous renal parenchyma.

two

transi-

tional cell carcinoma, one sarcoma, and three benign masses), nine had Doppler shifts under 2.5 kHz.

On

the

basis

of imaging

masses were assigned bility of malignancy, cy proved in 17 (85%).

were

assigned

malignancy

(14%).

Doppler

a low discovered

The

remaining

US in detecting

alone,

probability,

with one

43 masses

were

malignancy

in masses with these various possibilities for malignancy. the intermediate probability ry, Doppler detection of tumor nals was 58% sensitive (11 of

contrast Sonognam

spectrum

pretest Among categosig19) and

material of the

shows a 2-cm mass left kidney shows

of the left renal

96% specific renal

mass

(23 of 24) for

in the

demonstrates

malignant

masses.

DISCUSSION

20

a high probawith malignanSeven masses in only

(b)

This prospective series mass lesions demonstrates frequency Doppler-shifted

are renal nign port

encountered

(11,12). prior from (12),

in most

mass lesions renal masses. the conclusions

Our

of 70 renal that highsignals

malignant

yet are rare in beThese results supof earlier reports

current

study

and

our

retrospective study (1 1 ) differ that of Kuijpers and Jaspers based on the cutoff value we

recommended.

Whereas

seven

of

nine renal cell carcinomas had Dopplen shifts of 4 kHz or higher in their series (78%), only 1 1 of 24 carcinomas

Radiology

#{149} 705

a.

b.

Figure

Renal

6.

Doppler consistent

cursor with

cell carcinoma is on the malignancy.

inner

manifesting

C.

as microhematunia.

margin of the mass. (c) Left renal angiogram

(b)

(a) Sonogram

demonstrates

Doppler interrogation shows a hypervascular

of the mass mass (small

a 2-cm demonstrates arrows) with

isoechoic

left renal

mass

(arrows).

peak-systolic frequency an early draining vein

The

of 8 kHz, (large arrow).

in our current series had frequency shifts in this range (46%). Even if our two cases of miscellaneous malignancy were renal cell carcinomas, the sensitivity of using a cutoff level of 4

kHz would differences

increase between

may reflect the small the study of Kuijper

achieve

reasonably

to only 50%. these studies

The

sample size and Jaspers.

in To

high

sensitivity

for malignancy, we recommend a cutoff value of 2.5 kHz. This criterion provides high specificity (94%), with false-positive diagnoses limited to two cases of renal infection. Since renal infection is often clinically apparent, false-positive diagnoses based on Doppler investigation should be rare. Although comparison of renal mass Doppler signals to the main renab artery Doppler signals may be as useful as peak-systolic frequency for detection of malignancy (11), this approach may be less practical. First, an accurate sampling of the main renal

artery

was

occasionally

difficult

a.

b.

Figure

7. Renal gram demonstrates of the renal mass tinuous

waveforms

respiration,

carcinoma in a patient with benign prostatic hypertrophy. (a) Sonoa 4-cm hypoechoic right renal mass (arrows). (b) Doppler interrogation shows peak-systolic frequency of 3 kHz, consistent with malignancy. Conwere

such

difficult

as in this

to obtain

--

some

patients

who

were

unable

to suspend

HEMATOMA +

*

ANOIOMI’5 LOBATION

to

obtain, which may relate partially to operator dependence. Second, sampling the main renal artery increased study time without significantly improving accuracy. Doppler shift frequencies reflect the velocity of blood flow within a mass. Recent studies have demonstrated the histologic and angiographic presence of arteniovenous

in

case.

-

D I

I

cell

0

COLUMN

S 08

0 PEAK

2.5 SYSTOLIC

5 DOPPLER

7.5 SHIFT

Figure 8. Benign renal lesions cording to the clinical diagnosis uted according to peak-systolic shift frequency. ANGIOMYO poma.

(KHz)

divided acand distnibDoppler angiomyoli-

and hypervasculanity in masses with high Doppler frequency (9,10,12). Kuijpers and Jaspers noted that all seven renal cancers with Doppler shifts of 4 kHz on more were hypervascular or vascular at angiography, whereas two masses with

cular at angiography (12). Our study showed a similar but slightly weaker correlation of Doppler shifts with angiographic vasculanity. Correlation may not be perfect since Doppler fre-

whereas angiognaphic vasculanity is determined by the total volume of flow. We are currently performing a retrospective study to ascertain which specific angiognaphic features

shifts

quencies

may

shunts

706

of

2 kHz

#{149} Radiology

on

less

were

hypovas-

reflect

velocity

of

flow

correlate

most

closely

with

September

1990

high-frequency We conclude characterization sions.

We

tigation sion phy,

References

Doppler signals. that Doppler US aids of renal mass be-

recommend

whenever

Doppler

a renal

is encountered during since this additional

1.

exclude

malignancy.

Acknowledgment: knowledge statistical

Volume

Robert

The Lange,

sonogna-

analysis.

176

#{149} Number

3

gratefully for providing

Horii

2.

carcinomas:

cell dilemma.

BN.

discovery

Radiology

Bree

and

RL, Pollack

of

HM,

et al.

resolving

a

9.

1988;

excretory

L, et

imaging

features.

AJR

10.

6.

Fein AB, Lee JKT, Baife DM, et a!. Diagnosis and staging of renal cell carcinoma: a comparison of MR imaging and CT. AIR

7.

Quint LE, Glazer GM, Chenevert In vivo and in vitro MR imaging

1987;

11.

ap-

158: 1-10.

ac-

correlation and Radiology

1988; 169:359-362. Manotti M. Hnicak H, Fnitzsche P. Crooks LE, Hedgcock MW, Tanagho EA. Complex and simple renal cysts: comparative evaluation with MR imaging. Radiology 1987; 162:679-684. Taylor KJW, Ramos I, Carter D, Morse 55, Snowen D, Fortune K. Correlation of Doppler US tumor signals with neovasculan morphologic features. Radiology 1988; Taylor

KJW,

masses: Doppler Ramos Snowen

Ramos I, Morse 55, Fortune DO, Taylor CR. Focal liven differential diagnosis with pulsed US. Radiology 1987; 164:643-647. IM, Taylor KJW, Kier R, Burns PN, DP, Carter D. Tumor vascular

signals

in

KL, Hammers

1989;

MA. The current radiological to renal cysts. Radiology 1986;

proach

histopathologic sequence optimization.

166:57-62.

urogra-

phy/linean tomography, US, and CT. Radiology 1988; 169:363-365. Levine E, Huntrakoon M, Wetzel LH. Small renal neoplasms: clinical, patholog153:69-73. Bosniak

8.

1989;

Radiology

specificities

Reand

166:637-641. Warshauen DM, McCarthy SM, Street al. Detection of renal masses: sensitiv-

ic, and 5.

detection.

renal

AJ, Hul-

Raghavendra earlier

Small

ities

4.

SC,

Megibow

170:699-703. Amendola MA, diagnostic

3.

MA,

carcinoma:

increased

be-

U authors PhD,

DH,

nal-cell

investigation will add only a few minutes to the patient’s study. Furthenmore, duplex US should be considered to enable further characterization of equivocal mass lesions discovered at intravenous urognaphy, CT, or angiognaphy. In the absence of clinical evidence of infection, a Doppler shift frequency of 2.5 kHz or greater is a reliable indicator of malignancy. However, the absence of a high-frequency Doppler shift does not

SJ, Bosniak

nick

inves-

mass

tumors: pulse

Smith

12.

renal

masses:

detection

with

Doppler US. Radiology 1988; 168:633-637. Kuijpens D, Jaspens R. Renal masses: differential diagnosis with pulsed Doppler US. Radiology 1989; 270:59-60.

148:749-753.

TL, et al. of renal

Radiology

#{149} 707