Ultrasound scanning of the pelvis and abdomen for staging of gynecological tumors

21 Pages·2011·1.58 MB·English

UltrasoundObstetGynecol2011;38:246–266
PublishedonlineinWileyOnlineLibrary(wileyonlinelibrary.com).DOI:10.1002/uog.10054
Ultrasound scanning of the pelvis and abdomen for staging
of gynecological tumors: a review
D. FISCHEROVA
GynecologicalOncologyCentre,DepartmentofObstetricsandGynecology,FirstFacultyofMedicineandGeneralUniversityHospital,
CharlesUniversity,Prague,CzechRepublic
KEYWORDS: cervicalcancer;endometrialcancer;gynecologicaloncology;ovariancancer;staging;ultrasound;vaginal
cancer;vulvarcancer
ABSTRACT or mixed vascularity or displacement of vessels seems to
be the sole criterion in the diagnosis of metastatic or
This Review documents examination techniques, sono- lymphomatousnodes.
graphicfeaturesandclinicalconsiderationsinultrasound In the investigation of distant metastases, if a nor-
assessment of gynecological tumors. The methodology mal visceral organ or characteristic diffuse or focal
of gynecological cancer staging, including assessment of lesions(suchasasimplecyst,hepatichemangioma,renal
local tumor extent, lymph nodes and distant metastases, angiomyolipoma, fatty liver (steatosis)) are identified on
isdescribed. ultrasound, additional examinations using complemen-
With increased technical quality, sonography has tary imaging methods are not required. If, however, less
become an accurate staging method for early and characteristic findings are encountered, especially when
advanced gynecological tumors. Other complementary the examination result radically affects subsequent ther-
imaging techniques, such as computed tomography and apeutic management, an additional examination using a
magnetic resonance imaging, can be used as an adjunct complementary imaging method (e.g. contrast-enhanced
to ultrasound in specific cases, but are not essential to ultrasound, computed tomography, magnetic resonance
tumor staging if sonography is performed by a specialist imaging, positron emission tomography) is indicated.
ingynecologicaloncology. Copyright  2011 ISUOG. Published by John Wiley
Ultrasound is established as the method of choice &Sons,Ltd.
for evaluating local extent of endometrial cancer and
isthemostimportantimagingmethodforthedifferential
diagnosis of benign and malignant ovarian tumors.
INTRODUCTION
Ultrasound can be used to detect early as well as
locally advanced cancers that extend from the vagina, Ultrasound is a non-invasive, commonly available,
cervixorotherlocationstotheparacolpium,parametria, affordable imaging method associated with minimal risk
rectum and sigmoid colon, urinary bladder and other and discomfort to the patient. When performed by an
adjacent organs or structures. In cases of ureteric experienced diagnostician, it can play an invaluable
involvement, ultrasound is also helpful in locating the role in the primary diagnosis of gynecological cancers,
site of obstruction. Furthermore, it is specific for the the assessment of tumor extent in the pelvic and
detection of extrapelvic tumor spread to the abdominal abdominal cavity and the evaluation of treatment effects
cavity in the form of parietal or visceral carcinomatosis, as well as follow-up after treatment. Using ultrasound
omentaland/ormesentericinfiltration. to evaluate important prognostic parameters makes the
Ultrasoundcanbe usedtoassess changesininfiltrated individualization of oncology treatment possible. In this
lymph nodes, including demonstration of characteristic way we can make maximum therapeutic impact with
sonomorphologic and vascular patterns. Vascular pat- minimal patient morbidity. Ultrasound also enables the
terns are particularly well visualized in peripheral nodes targetedbiopsyofadvancedtumorsormetastaticlesions,
using high resolution linear array probes or in the pelvis allowingfastandminimallyinvasiveestablishmentofthe
using high-frequency probes. The presence of peripheral tumorhistology1.
Correspondenceto:DrD.Fischerova,DepartmentofObstetricsandGynecology,FirstFacultyofMedicineandGeneralUniversity
Hospital,Apolinarska18,12851Prague2,CzechRepublic(e-mail:daniela.fi[email protected])
Accepted:8April2011
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. REVIEW
Ultrasoundstagingofgynecologicaltumors 247
The accuracy of ultrasound is largely dependent on
three variables: operator, equipment and patient. To
become an ultrasound expert in gynecological oncology
requires adequate practical expertise,whichis developed
through exposure to abnormal findings. It is of utmost
importance to use complementary imaging methods in
questionable cases and/or to be present in the operating
theater in order to maximize one’s knowledge of the
tumor’scharacteristicsandspread.
Toexaminetheoncologypatient,ahigh-endultrasound
machine equipped with sensitive Doppler and endocav-
itary (microconvex) and transabdominal (convex array
probeforabdomenandlinearprobeforperipherallymph
node assessment) transducers is needed. In addition, the
ultrasoundfindingsshouldbestored,intheformofstatic
images taken in standard sections, videoclips or three-
dimensional volumes, for subsequent additional offline
analysis,ifnecessaryinconsultationwithanexpert.
The last significant variable is the patient. Although
over the last few years there has been considerable
improvement in scanning technology, there are still lim-
itations in some cases (e.g. obese patients and retroperi-
toneumevaluation,extensiveascitesandliverassessment,
postoperative adherent intestinal loops causing acous-
tic shadowing). In such cases a complementary imaging
method or diagnostic laparoscopy can be used to obtain
further information, if this is relevant to the patient’s
management.
Figure1 Pelvicanatomyasseenontransvaginalortransrectal
ULTRASOUND EXAMINATION sonography(sagittalview)duringprobeinsertion,includingdetails
TECHNIQUE ofbladderandrectalwall.1,Urethra;2,bladder;3,ureterovaginal
space;4,vesicocervicalspace;5,vesicouterinepouch;6,vagina;
All gynecological oncology patients should be examined 7,uterus;8,Fallopiantube;9,ovary;10,rectovaginalspace;11,
systematically and carefully using a combination of rectum(11A,retroperitonealpart;11B,intraperitonealpart;11C,
mesorectum);12,pouchofDouglas(rectouterinepouch);
endocavitary sonography, with a microconvex array
13,sigmoidcolon;14,sigmoidmesocolon;15,smallintestine
probe inserted transvaginally or transrectally (Figure1),
(ileum);16,mesenteryofsmallintestine(rootofmesentery);17,
and transabdominal sonography, with a convex array mucosa;18,muscularlayer;19,rectalvisceralfascia;20,serosa(a
probe for evaluation of possible tumor spread in the reflectionoftheperitoneum).
abdominal cavity and with a linear array probe for
examiningtheperipherallymphnodes(Figure2). require any special bowel preparation such as an enema
Transvaginal ultrasound is the optimal approach or glycerine suppository. The patient is informed about
for examining the uterus (including uterine zonal the transrectal insertion of the probe, and the procedure
anatomy:cervix,endometrium,junctionalzone(endome- is then performed with the patient in an identical posi-
trial/myometrialborder),myometrium,perimetrium),the tion (supine, with elevated pelvis) and with an identical
adnexa and the pelvic peritoneum (Figure3, Table S1). probetothatusedforatransvaginalprocedure.Guiding
Transrectal insertion of the probe has an advantage in the probe into the rectum via the anus is accomplished
patients who are virgo intacto, have a stenotic vagina throughcoordinatedmovementoftheprobeintheexam-
or have undergone brachytherapy, in whom transvagi- iner’srightandlefthands.Theindexfingerofthelefthand
nalinsertionisnotpossible(VideoclipS1).However,the openstheanusbyexertinggentlepressureonthebaseof
main use of the transrectal approach is for the detection theposteriorcommissurewhiletheprobeisinsertedinto
of locally advanced tumors of the vulva, as well as early the anus by gently depressing the anterior commissure.
andadvancedvaginalandcervicalcancer(Figure4,Table If the anal sphincter is constricted, the patient may be
S1,VideoclipS2).Inthesecases,thetransrectallyinserted instructedtoperformtheValsalvamaneuver.
probe allows for the detection of tumor spread into the Fortransabdominalsonography,aconvexarrayprobe
paracolpium, parametrium, and vesicocervical, vesico- (3.5–7MHz) is usually used, depending on the patient’s
vaginal and rectovaginal spaces and the urinary blad- body habitus.Anultrasoundexaminationof theabdom-
der and rectum. Transrectal sonography also eliminates inal cavity has to be performed systematically and the
theriskofbleedingfromanexophyticallygrowingtumor entire anatomy has to be evaluated in both sagittal and
of the vagina or uterine cervix. The technique does not transverse sections, which is accomplished by rotating
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. UltrasoundObstetGynecol2011;38:246–266.
248 Fischerova
Figure3 Examplesofindicationfortransvaginalsonography.
1,Uterinetumor;2,adnexalmass;3,peritonealtumor.
Figure2 Anatomyasseenontransabdominalsonography,with
evaluationofvisceralorgans,peritonealsurfacesincluding
omentumandlymphnodessurroundingthemainandvisceral
vessels.1,liver;2,spleen;3,kidney;4,greateromentum(4A,
supracolicpart;4B,infracolicpart);5,femoralvessels(5A,femoral
artery;5B,femoralvein);6,iliacvessels(6A,externaliliacartery;
6B,externaliliacvein;6C,internaliliacartery;6D,commoniliac
artery);7,aorta;8,inferiorvenacava;9,sigmoidcolon;10,
descendingcolon;11,transversecolon;12,ascendingcolon.
◦
the probe 90 . It is helpful to memorize the order of the
stepsneededtocompleteafulltransabdominalultrasound
examinationtoensureitisperformedidenticallyeachtime
andthuspreventanyomissions.First,attentionispaidto
thevisceralorgansintheupperabdomen(suchasthekid-
neysandadrenalglands,spleen,liverandpancreas);their
sizeandstructureisevaluatedandpossibleintraparenchy-
matous focal or diffuse lesions, capsular infiltration or
visceral lymphadenopathy are described (Figure5). Sec-
ond, the parietal, visceral, mesenteric peritoneum and
omentum are evaluated, as there is potential for tumor
spread in the form of parietal (lateral paracolic gutters,
diaphragm, anterior abdominal wall), omental, visceral
(intestinal carcinomatosis, organ surfaces) or mesenteric
(mesenteryofsmallintestineormesocolon)carcinomato-
sis. Finally, the peripheral(superficial and deep inguinal)
andretroperitoneal(alsocalledparietal)lymphnodesare
evaluated. In experienced hands, the usual duration of Figure4 Examplesofindicationfortransrectalsonography.
1,Advancedvulvalcancer;2,vaginalcancer;3,cervicalcancer.
a systematically performed combination of transvaginal
(or transrectal) and transabdominal scans to define the
clinicalstageofdiseaseisapproximately15min. visibility of organs located partially within the rib cage
Ultrasonographyisadynamicprocedureduringwhich maybeimprovedbydeepinspirationandslowexpiration.
the possibility of additional functional tests can provide The patient also provides important information on
important information (Videoclip S3)2. The acoustic tenderness during the examination (e.g. level of pain
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. UltrasoundObstetGynecol2011;38:246–266.
Ultrasoundstagingofgynecologicaltumors 249
of a tumor mirrors its biological behavior; tumors with
a higher density of newly formed vessels are usually
more aggressive, form lymphatic metastases early and,
therefore, tend to be of a higher FIGO stage3–6. When
performing a color Doppler examination, a subjective
semiquantitative assessment of blood flow is made as
follows:a score of 1 is givenwhen no blood flow can be
observed in the lesion; a score of 2 is given when only
minimalflow can be detected;a score of 3is givenwhen
moderate flow is present; a score of 4 is given when the
massappearshighlyvascularized7.
Another possibility that may increase the sensitivity
andspecificityofultrasonographyistheuseofultrasound
contrast media (contrast enhanced ultrasonography),
especiallyforthedifferentialdiagnosisofhepaticlesions.
This, however, requires special ultrasound software
as well as intravenous use of the suspension and,
therefore, the advantages of ultrasound as a readily
available, affordable and non-invasive method are
compromised8.
PRIMARY GYNECOLOGICAL TUMORS
(TNM STAGING)
When a tumor is limited to the organ of origin, special
attention must be paid to a careful description of
Figure5 Stepsinvolvedintransabdominalsonography. prognostic parameters essential for individualization of
1,Evaluationofvisceralorgans;2,assessmentofperitoneal treatmentandchoiceoftherapeuticmodality(TableS2)9.
surfaces,includingomentum;3,detectionofinguinaland
Ultrasoundalsohasaroletoplayinthepreciseevaluation
retroperitoneallymphadenopathy.Probepositionisindicatedby
orangeandgreenbarsandprobemovementbyarrows. of advanced tumors (Table S2) that spread either
locally, through infiltration of surrounding structures
(paracolpium,pericervicalfasciaandparametria,urethra,
during vaginal examination of various pelvic structures, urinary bladder, rectosigmoid), and/or in the form of
sonopalpationoflivertodetermineadullpainduetothe peritoneal lesions in the pelvis and abdominal cavity
involvementorstretchingofthelivercapsuleintheevent (carcinomatosis).Inaddition,thetumorcouldalsospread
of metastatic spread to the liver). It is also important through the lymphatic and vascular system, as described
to evaluate the mobility of organs in order to exclude bytheTNM(primaryTumor,regionallymphNodesand
adhesions,toobservethemovementofatumorrelativeto distantMetastasis)stagingclassificationsystemdeveloped
anorganinordertodeterminethetumororiginand/orto by the International Union Against Cancer (UICC) and
observemovementoffluidwithinthepelvisorabdominal theAmericanJointCommitteeonCancer(AJCC)10.After
cavity or within a tumor itself. The inherent movement the T, N and M categories are assigned, they can be
of the target organ may also be used, for example further grouped into Stages I–IV according to the FIGO
when assessing gallbladder content, or when trying to stagingsystemdevelopedbytheInternationalFederation
distinguish between intestinal loops and an infiltrated of GynecologyandObstetrics.The revisedFIGOstaging
omentumbasedonthepresenceorabsenceofperistalsis. published in 2009 should be used for determining the
Intestinal peristalsis may even be provoked through clinicalandsurgicalstagingingynecologicaloncology11.
repeated pressure exerted by the probe (Videoclip S3).
Sonopalpationofthelivernotonlyevaluatesitstenderness
Assessmentofprimarytumorconfinedtotheorgan
(capsule tension-related pain, dull pain) provoked by
oforigin(T1NM)
contact of probe with the organ but can also assess its
consistencyintheeventthatlivercirrhosisissuspected.
Vaginalcancer
Morphologicalcharacterizationmaybecomplemented
by Doppler ultrasonography to assess the presence, Method: combination of transrectal sonography in both
architectureanddensityofnewlyformedvessels.Doppler sagittalandtransverseplanes
is also useful to confirm the size of isoechogenic On ultrasound, the vagina is delimited ventrally and
(less sonomorphologically pronounced) tumors, and to dorsallybyhyperechogenicvisceralfascia.These,together
evaluate changes in tumor viability after treatment with vesical or rectal fasciae, form the hypoechogenic
(post-irradiation or post-chemotherapy changes versus vesicovaginal and rectovaginal spaces, which are filled
persistent viable tumor). In general the vascularization withareolarconnectivetissue.Thehyperechogenictissue
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. UltrasoundObstetGynecol2011;38:246–266.
250 Fischerova
alongthesideofthevaginauptothelevelofthevaginal
fornixattachmenttothecervixisnamedtheparacolpium
and consists of connective mesenteries enveloping the
vaginalandtheinferiorvesicalvessels.Ultrasoundshould
distinguish between tumors limited to the vaginal wall,
i.e. Stage-I tumors, and locally advanced tumors, as the
latterrequiremoreextensivetreatment(FigureS1).
Cervicalcancer
Method:transrectalortransvaginalsonographyinsagittal
andtransverseplanes
The sonographic detection rate for cervical cancer is
93–94%12,13andultrasoundisahighlyaccuratemethod
in classifying early-stage tumors12–15. It is important
to focus on the following information required from
the ultrasound examiners by the clinicians who will be
planning the individual treatment of a patient. First,
the presence of a tumor and its topography/growth
pattern (exocervix/exophytic tumor growth (FigureS2),
endocervix/infiltrative tumor growth (FiguresS3–S5))
need to be assessed. The tumor size is measured in
three diameters (FigureS6). The next step is especially
important for young patients requiring a fertility-sparing
procedure16: it must be determined whether the distance
between the tumor and the internal cervical os is
sufficiently large (≥10mm) to maintain an adequate
tumor-free margin and reduce the risk of future
miscarriage (FigureS7)17,18. The third priority for an
Figure6 Transvaginal/transrectalsonographicmeasurementof
ultrasound examiner is to evaluate the extent of tumor
tumor-freestromaincervicalcancer:measuringthedistance
stromal invasion. The proportion of stromal invasion
betweencervicaltumorandpericervicalfascia(PCF)allows
can be defined as either partial (≤2/3 or >2/3) or full- individualizationoftreatmentwithrespecttothedegreeof
thickness or, more precisely, it can be defined based extensionlaterallyduringparametrectomyintheeccentrically
on the measurement of tumor-free stroma (FigureS8, locatedtumor.(a)Tumor–PCFmeasurementventrallyanddorsally
inthesagittalviewineccentricallylocatedtumor;(b)tumor–PCF
Figure6). This is achieved by measuring the distance
measurementintransverseview.Redcircleshowsextentof
between the tumor and the pericervix, or pericervical
requiredparametrectomyaroundthecervicalcancer.1,Urinary
fascia (dense hyperechogenic tissue surrounding the bladder;2,cervicalcancer;3,rectum;4,ventralparametrium;5,
cervix), at the point where the ventral (including lateralparametrium;6,dorsalparametrium;7,autonomic
vesicouterine and vesicovaginal), lateral and dorsal nerves/hypogastricplexus;dotteddouble-headedarrows
correspondtothedistancesbetweentumorandpericervicalfascia
(includinguterosacralandsacrovaginal)ligamentsattach
measuredatpointswhereparametriaarise.Notethatthe
to the cervix on both sides. The extent of the radical
parametriaareaccompaniedbyautonomicnervesthatremain
procedure (parametrectomy) can then be planned, based intactduringthelessradicalprocedure,withlessseriousside
on these data19. For example, in FigureS8, the tumor effects.
almost reaches the pericervical fascia on the right
side and, therefore, extended radical parametrectomy information regarding the tumor location, size (three
is required. On the contralateral side, a less radical diameters), sonomorphology (e.g. echogenicity, homo-
procedure is needed because the tumor does not extend geneity, endometrial–myometrial junction) and vascular
into the pericervical fascia. If the pericervical fascia pattern20.Moreover,itoffersthepossibilityofevaluating
is infiltrated by tumor, the degree of parametrial theextentoftumorinfiltrationintothemyometriumand
involvement is graded according to the scale introduced towards the cervix. Ideally, the depth of tumor invasion
inTableS3. should be measured from the endometrial–myometrial
interface to the deepest edge of the tumor extension into
the myometrium and should be related to the width of
Endometrialcancer
the normal myometrium. However, sonographic mea-
Method: transvaginal sonography in sagittal and trans- surement has its limitations: in some cases the normal
verseplanes myometrium is not accessible as it is either consumed
Ultrasound is widely accepted as the appropriate stag- by the tumor or greatly thinned by pressure from exo-
ing method for early-stage endometrial cancer9. Sono- phytically grown tumor. Another means of measuring
graphic diagnosis should provide the clinician with the degree of myometrial infiltration is to determine the
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. UltrasoundObstetGynecol2011;38:246–266.
Ultrasoundstagingofgynecologicaltumors 251
relationshipbetween the maximum tumor thickness (d1)
andtheanteroposteriordiameteroftheuterus(d2)inthe
sagittalplane.Invasionoflessthanhalfthemyometrium
is recorded when the ratio of d1 to d2 is <50% (Stage
T1a), and invasion equal to or greater than half the
myometriumisrecordedwhentheratioofd1tod2equals
or exceeds 50% (Stage T1b)21. This approach seems less
operator-dependent,althoughtheextentofinvasionmay
be overestimated in cases of large polypoid exophytic
tumors with intact but thinned myometrium. Both tech-
niqueshaveover80%accuracyinassessingtheextentof
myometrial infiltration21–23. Another option is to mea-
sure instead the shortest myometrial tumor-free distance
totheserosa.Thisparameteriseasilyassessedandseems
alsotobeausefulprognosticfactorforrecurrence,using
a cut-off of 10mm (area under the receiver–operating
characteristicscurve,0.76)24.
In addition, power Doppler can be useful to assess
the vascular pattern. For example, the presence of
abnormal perfusion permits better detection of the
tumor border in less visible tumors (i.e. those that
are ischoechogenic with the myometrium). The presence
of adenomyosis is accompanied by normal myometrial
Figure7 High-riskendometrialcancer:summaryofnegative
perfusion, while a circular vessel pattern helps to
prognosticfactors.
differentiate myomas. Moreover, in cases of mainly
polypoid growing tumors, the detection with Doppler
tumors, but in contrast to vulval, vaginal, cervical and
of dominant feeding vessels enables more detailed
endometrial cancers, the biopsy results are not known
examination of the endometrial–myometrial junction at
priortosurgery.Wemustkeepinmindthepotentialrisk
theinsertionofthepedicle(entrypointoffeedingartery)
of tubal cancer, for example in cases of solid ‘sausage-
inordertoassessmoreaccuratelythedepthofmyometrial
like’ (FigureS11) or fibroma-like (FigureS12) perfused
invasion(FigureS9).
structures near the ovary, or in cases of hydrosalpinx
In order to exclude cervical stromal involvement, it
containinga solidareawithrichvascularity(FigureS13)
is important to visualize the level of the uterine artery
(Figure8).
entries into the uterus. By shifting the probe from
side to side to assess the whole uterus in the sagittal
Ovariancancer
plane, the level of entry of the left and right uterine
arteries can be determined by Doppler. This level cor-
Method: transvaginal sonography in sagittal and trans-
responds approximately to the internal cervical os. In
verseplanes
cases in which the endometrial tumor only protrudes
High-quality ultrasound is, in most cases, the imag-
intothecervicalcanalandhasnotinfiltratedthecervical
ingmethodofchoicewithrespecttothecharacterization
stroma, by applying slight pressure with the transvagi-
of adnexal masses. Increased size, the presence of solid
nal probe the sliding effect of tumor mass against the
papillaryprojections,ahighcolorscoreaswellasthepres-
endocervical mucosa can be observed. Figure7 and
ence of a highly vascularized solid component within an
FigureS10 summarize the sonographic negative prog-
adnexalmassareallfindingsthatmaybeassociatedwitha
nostic factors for recurrence of endometrial cancer and
diagnosisofmalignancy(FiguresS14andS15).Theopti-
eventual survival25. These high-risk endometrial cancers
malmethodforassessing thelikely pathology ofa pelvic
present on ultrasound as large hypoechogenic or mixed
mass is ultrasonography by an expert; however, mathe-
tumors located in the isthmus/fundus/whole uterus, with
maticalmodelshavebeendevelopedthathaveperformed
multiple global vessels entering them via the endome- toasimilarlevelonexternalvalidation27.Whenconsider-
trial–myometrial border, with deep extension into the ing fertility-sparing surgery, using ultrasound to exclude
myometriumandeventuallythecervicalstroma26(Video- the possibility of tumor spread through the ovarian cap-
clipS4). suleandtoconfirmthatthecontralateralovaryisnormal
mayallowthecontralateralovarytobeleftinsituwithout
theneedforanintraoperativebiopsy(FigureS16).
Tubalcancer
Method: transvaginal sonography in sagittal and trans-
Assessmentoftumorextension(T2–T4NM)
verseplanes
A patient’s prognosis is affected significantly if early- Whilst ultrasound has been accepted as the technique
stagetubalcancerisproperlydiagnosed.Aswithovarian of choice for the assessment of gynecological tumors
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. UltrasoundObstetGynecol2011;38:246–266.
252 Fischerova
Figure8 Examplesoftubalcancerasseenontransvaginalsonography.Schematicdiagrams(a–c)withcorrespondingultrasoundimages
(d–f)showing:(a,d)earlytubalcancermanifestedassolid‘sausage-like’perfusedstructureneartheovary;(b,e)perfusedsolidlesioncloseto
theovary(note,incontrasttoafibroma,thislesionishighlyperfusedandlacksechogenicstripes);(c,f)hydrosalpinxwithaconcurrentsolid
vascularizedlesion.
limitedtotheorganoforigin,itisbecomingincreasingly Parametrialinfiltration
recognized that ultrasound is important for individual
Method:transrectalsonographyortransvaginalsonogra-
treatment planning in locally advanced gynecological
phyinbothsagittalandtransverseplanes
tumors involving adjacent pelvic organs, as well as for
Assessment of parametrial infiltration must be
assessingtumorextentwithintheabdominalcavity,when
approachedinastandardizedmanner.Itisusefultostart
inthehandsofanexperiencedultrasoundexaminer.There
withamidsagittalplaneattheleveloftheectocervixupto
isasignificantamountofevidencerelatingtoultrasound
theuterineisthmus;theprobeisthengraduallymovedto
examination of early-stage gynecological tumors. Much
the right from the midline (FigureS17a–c, Videoclip S5)
less has been published about sonography of more
toobservetheventral,dorsalandlateralrightparametria.
advanced tumor stages, which will, thus, be the focus
Next, the probe is moved backwards in the same way
oftheinformationprovidedbelow.
and continues from there to the left side of the pelvis
◦
(firststep).Rotatingtheprobethrough90 counterclock-
Infiltrationoftheparacolpium
wise and shifting from the urinary bladder towards the
Method:transrectalsonographyinsagittalandtransverse rectum (FigureS17d–f) shows the urinary bladder wall,
planes the ventral parametria, the cervix and lateral and dorsal
In the event of tumor spread into the vagina or when parametriaandtherectum(secondstep)(Figure10).
a primary vaginal tumor is diagnosed, it is important Standard clinical examination of the parametrium
for surgical planning to determine whether the tumor usually gives inaccurate results, especially in cases of
is limited to the vaginal wall or whether it has already incipient parametrial infiltration in obese patients or
penetratedthevisceralfasciaeventrallyordorsallyandis patients with bulky tumors. In contrast, the accuracy
growing into the vesicovaginal/rectovaginalspace and/or oftransrectalsonographyforthedetectionofparametrial
is invading the surrounding tissues (paracolpium) later- involvement is comparable to that of MRI (98.9% vs
ally. The presence of hypoechogenic tumor prominences 94.7%,P≤0.219)12.Forclinicalpurposesitisimportant
into the hyperechogenic connective tissue of fasciae to discern whether the pericervical fascia is infiltrated,
or paracolpium should be assessed in both transverse and to describe the topography precisely. Currently,
and sagittal views on transrectal sonography (FigureS1, we are advised to use the international anatomical
Figure9).Althoughthetermparacolposisfrequentlyused nomenclature, although this is not always what happens
in pelvic oncology surgery, this structure is not officially in the surgical literature and in daily use28–30. In
recognized in the international anatomical nomenclature international anatomical nomenclature, ‘parametrium’
andisclassifiedaspartoftheparacervix28,29. refers to tissues that surround the uterine artery between
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. UltrasoundObstetGynecol2011;38:246–266.
Ultrasoundstagingofgynecologicaltumors 253
any direction, ventrally affecting the vesicouterine and
vesicovaginal ligament (otherwise referred to as ventral
parametrium) and/or dorsally affecting the uterosacral
and sacrovaginal ligament (otherwise referred to as
dorsal parametrium). Although the consensus of new
anatomicalterminology was reachedmore than10years
ago, surgeons are reluctant to abandon the unofficial
but traditional terminology (ventral, lateral and dorsal
parametrium)31.
Becausepreciseevaluationoftheextentofparametrial
tumor involvement into ventral/lateral/dorsal parametria
is so important for clinical practice, we adopted a
five-level grading scale to assist in treatment planning
(FiguresS18–S20,TableS3,Figure11).Thewell-defined
hyperechogenic line surrounding the cervical stroma is
described on ultrasound as the pericervix or pericervical
fascia. However, on the lateral sites where the lateral
parametriumisattachedtothecervixandtheuterineand
otherparametrialvesselsenterthecervix,thepericervical
fascia is not properly visualized. At this point the
parametrial involvement is manifested as hypoechogenic
irregulartumorprominencesintothelateralparametrium,
which has to be differentiated from the cervical vascular
plexuses using color or power Doppler. In the case of
advanced cervical cancer, we must distinguish whether
the tumor only infiltrates the pericervical fascia (Grade
1), whether it progresses continuously through the
pericervical fascia to the parametrium (Grade 2–3), or
whether it spreads non-continuously in the form of
Figure9 Vaginalcancerasseenontransrectalsonographyin
‘skip’ metastases in the lateral parametrium (Grade 4).
sagittal(a)andtransverse(b)views.Alongwithventralanddorsal
Skip metastases (i.e. visceral parauterine lymph node
shifting,theprobeisalsousuallymovedslightlytotherightorleft
towardsanareaofinterest.Thearrowsin(b)indicatemovementof metastases)arepicturedashypoechogenicroundedlesions
theprobesshownin(a).Notethatinthesagittalview,thecancer that need to be evaluated in both sagittal and transverse
doesnotseemtobeinfiltratingthevaginalwall;however,thetrans- planes to avoid confusing them with the hypoechogenic
verseviewconfirmsthatthetumorextendstotheparacolpium.
image of cervical vascular plexuses. In addition to their
precise topography, the size of infiltrated parametrial
ligamentsismeasuredinthreedirections.
the uterine corpus and pelvic sidewall cranial to the
ureter and superficial uterine pedicle. The dorsolateral
attachment of the cervix is named the ‘paracervix’, and
Involvementofurinarybladder
thistermshouldreplaceotherssuchascardinalligaments,
ligaments of Mackenrodt, lateral cervical ligaments and Method:transrectalortransvaginalsonographyinsagittal
parametrium. Moreover, cervical cancer can spread in andtransverseplanes
Figure10 Techniqueofparametrialevaluationbytransrectalsonographyinsagittalandtransverseviews.(a)Firststep,sagittalview:
shiftingoftheprobe(blueandgreenarrows)frommidlinetorightandleft;(b)firststep,transverseview;(c)secondstep,sagittalview:
rotationoftheprobe90◦counterclockwiseandevaluationofparametriabyshiftingtheprobefrombladdertowardsrectum;(d)second
step,transverseview.Notethat,alongwithventralanddorsalshifting,theprobeisalsousuallymovedslightlytotherightorlefttowards
anareaofinterest,i.e.eithertherightortheleftparametrium.
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. UltrasoundObstetGynecol2011;38:246–266.
254 Fischerova
Figure11 Gradingofparametrialinfiltrationbytransvaginal/transrectalsonography.(a–c)Schematicdiagramsshowing:(a)intact
pericervicalfascia(PCF)(Grade0),lateralparametria(lateralp.)andPCF;(b)parametrialinfiltrationGrade1(disruptedPCFbutwithout
progressionthroughthefasciaintoparametria)andGrade2(incipientinfiltrationofPCF);notethattheincipientinfiltrationischaracterized
bydiscretebreaksinthePCFwithveryfinehypoechogenicprominencesintotheparametria;(c)nodularinfiltration(Grade3)and
discontinuousparametrialinfiltration(Grade4).(d–i)Ultrasoundimagesshowing:(d)inthesagittalview,hyperechogenicPCF(Grade0)
locatedbetweenthecervixandhyperechogenicbladdervisceralfascia(blackdashedlinecorrespondstothevesicocervicalspacealsoknown
astheseptum);(g)inthetransverseview,intactPCFsurroundingthecervicalstromadorsally;(e,f,h,i)parametrialinfiltrationGrades1–4.
The extent of primary tumor spread into the urinary Inaddition,anevaluationoftheintegrityoftheurinary
bladderand/orrectumcanbedeterminedsimultaneously bladder wall can be obtained through a functional test,
and the level of infiltration in both is graded identically wherebyexertingpressurewiththeprobeontheanterior
(Figure12). Ultrasound provides more detailed informa- vaginal wall determines the mobility (sliding) of the
tion on bladder involvement than does cystoscopy, as bladderagainsttheuterinecervix2.
this canonly show bullous mucosaledema inthe case of
tumor infiltration reaching the submucosa, or polypous
Rectum/rectosigmoidinfiltration
changes of the urinary bladder mucosa. In clinical prac-
tice,differentclassificationsareestablishedwithregardto Method:transrectalortransvaginalsonographyinsagittal
the depth of tumor invasion32. It seems to be sufficient andtransverseplanes
todistinguishwhetherthetumorreachestheexternal(or While in clinical practice the ultrasound staging of
outer) hyperechogenic layer of the bladder, which corre- rectal carcinoma requires a precise evaluation of the
sponds to the vesical fascia, or continues to spread into tumor spread through different layers of the rectal wall
thehypoechogenicbladderwallmusclelayer,orwhether towardsthemucosa,ingynecologicaloncologyasimpler
itgrowsintothehyperechogenicmucosa.Weadoptedthis classification scheme is sufficient. This resembles the one
three-pointinvasionscoreandpresentit inTableS4and usedfordescriptionoftumorspreadthroughtheurinary
inFiguresS21–S23. bladderwall(TableS4,Figure12).
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. UltrasoundObstetGynecol2011;38:246–266.
Ultrasoundstagingofgynecologicaltumors 255
Figure12 Gradingofbladderand/orrectaltumorinfiltrationasseenontransvaginal/transrectalsonography.(a)Grade1(infiltrationof
hyperechogenicbladderand/orrectalfascia);(b)Grade2(infiltrationofhypoechogenicmusclelayer);(c)Grade3(infiltrationof
hyperechogenicmucosaandintraluminaltumornodule).
Inhealthyindividuals,allpelvicorgansaredemarcated Especiallyinlocallyadvancedcervicalcancers,extrinsic
subperitoneally against the rectal wall by a narrow obstruction of the distal part of a ureter may be encoun-
echogenic stripe of fibrous and fat tissue: the visceral tered(FigureS20d).Theuretercanbecomecompressedor
fascia. Gynecological tumors (from vagina, cervix and infiltratedwhere it touches the vasa iliaca inthe event of
other locations) infiltrate first the hyperechogenic layer massive lymphadenopathy, or through tumor infiltration
that reflects their visceral fascia, then the hypoechogenic of the ventral/lateral/dorsal parametrium. If the obstruc-
rectovaginal space (also known as rectovaginal septum, tionisinthevicinityofthebladder,themegaureterandits
posterior vaginal fascia or Denonvillier’s fascia) that peristalsiswilleventuallybevisualizedbyanendocavitary
extends inferiorly between the cervix and vagina probe inserted transvaginally or transrectally (Videoclip
(ventrally) and the rectum (dorsally). Subsequently, the S6). Transabdominal ultrasonography can be used to
tumors spread through the hyperechogenic rectal fascia followadilatedureterfromthekidneytothepelvis.
intoitshypoechogenicmuscularlayerandhyperechogenic Ureteral dilatation may be accompanied by distention
mucosa into the lumen (FiguresS24–S26, Table S5). As of the renal sinus (Grade 1, FigureS28), distention of
withurinarybladderwallinfiltration,knowingtheextent the renal pelvis and calyces (Grade 2, FigureS29) and
ofrectalwallinvolvementcouldmodifymanagement,for by sacciform hydronephrosis followed by atrophy of the
example choice of radiotherapy type that will reduce the renal parenchyma (Grade 3, FigureS30a,b, Figure13).
riskoforganfistuladevelopment. The degree of hydronephrosis depends on the duration
After emerging from the pouch of Douglas, the rec- and type of the obstruction (partial or complete) (Table
tum is no longer positioned subperitoneally; it is sur- S6). In advanced cervical cancer, hydronephrosis is usu-
rounded by peritoneum that could form a mesorectum ally an asymptomatic finding and may be either uni- or
and, at about 15–20cm from the anus in the mid- bilateral, depending on the type of parametrial infiltra-
sacral region, it reaches the sigmoid colon where it is tion. Transabdominal ultrasound is an efficient method
still wrapped in the peritoneum that now forms the for assessing the presence or absence of hydronephrosis.
sigmoid mesocolon, attaching the sigmoid colon to the In certain cases, the dilated ureter is visualized as far as
posterior abdominal wall (Figure1). Advanced tumors thepelvis,butfromthatpointonwardsitismoreadvan-
of the ovary and Fallopian tubes, and primary peri- tageoustouseanendoluminalprobetoidentifypartialor
toneal tumors not only spread along the subperitoneally completeureteralobstructionindetail(FigureS30c).High
positioned rectal wall, where they usually infiltrate the accuracy inthe sonographic diagnosis of hydronephrosis
rectovaginalspace(FigureS24b,c),butalsoreachtheperi- andpossiblyalsoidentificationoflocationoftheobstruc-
tonealsurface of the rectumand the sigmoidinthe form tionallowsfortimelyinterventioninordertopreventthe
of metastatic implants, with infiltration of the intesti- developmentofanon-functionalkidney.
nal hyperechogenic layer (serosa), hypoechogenic layer
(more deeply located muscle layer), or, in rare cases, the
intestinal mucosa, where they bulge into the lumen of Implantmetastases(carcinomatosis)
the intestine (FigureS27). Knowing whether the wall of
the rectosigmoid is infiltrated by an advanced ovarian Method:combinationoftransvaginalandtransabdominal
cancer is essential when planning the extent of primary sonographyinbothsagittalandtransverseplanes
cytoreductivetreatment. The peritoneum that lines the walls of the
abdominopelvic cavity (parietal peritoneum) invaginates
at certain points, with an organ inside each invagina-
Hydroureterandhydronephrosis
tion(visceralperitoneum).Ifthisinvaginatedperitoneum
Method:combinationoftransvaginalandtransabdominal comes in contact with itself, it forms the organ’s mesen-
sonographyinbothsagittalandtransverseplanes tery. For example, the mesentery suspends the jejunum
Copyright2011ISUOG.PublishedbyJohnWiley&Sons,Ltd. UltrasoundObstetGynecol2011;38:246–266.