Article - Postgraduate Medical Journal · enough of the beam to prevent sound transmission...

Postgraduate Medical Journal (1987) 63, 525-532

Review Article

Pitfalls in the ultrasonographic diagnosis of gallbladderdiseases

E.J. Fitzgerald' and A. Toi2*

'Department ofDiagnostic Radiology, University Hospital of Wales, Heath Park, CardifCF4 3XW, UK,and 'McMaster University Medical Centre, Hamilton, Ontario, Canada.

Summary: Ultrasonography is rapidly replacing radiological techniques of gallbladder investigation.While ultrasonography is highly accurate, there are technical, anatomical and diagnostic pitfalls whichwill trap the unwary. This presentation highlights the pitfalls which we have encountered, reviews theliterature in this area and suggests techniques whereby these pitfalls may be avoided.

Introduction

Ultrasonography is now considered by many to be themethod of choice of screening for gallbladder disease.The accuracy of this technique is claimed to exceed90%.' ,2,3, However, high false positive rates of7% andfalse negative rates of 15% are still reported in someseries.4'5 Since the diagnosis of gallstones by ultrason-ography is often followed by cholecystectomy withoutfurther confirmatory studies, the avoidance, especiallyoffalse positive diagnosis is important. If false positivegallbladder diagnosis were to occur at the 1.5% ratereported by Allen-Mersh,5 then about 2,000 unneces-sary cholecystectomies could occur in England andWales alone, and 7,000 in the United States.We have not been able to find any article listing the

myriad of problems encountered at ultrasonographicinvestigation of the gallbladder and as a result wepresent the pitfalls and problems which we haveexperienced over the past eight years at our institu-tions and found quoted in other publications, andsuggest methods to overcome these problems.

Discussion

The types of problems may be broken down roughlyinto three major groups: technical, anatomical anddiagnostic. Technical problems relate to choice and

Table I Pitfalls in the ultrasonographic diagnosis of gall-bladder disease

Technical:1. Mis-identification: bowel for gall stone

ligamentum tereshepatic granulomasaortamigrating masses (dermoid)

2. Wrong technique: transducer, gainpatient not moved

3. Pseudosludge and calculi due to side lobe artefact.4. Communication: typographical and documentation

errors

Anatomical andphysiological variants1. Gallbladder folds junctional fold

valves ofHeisternarrow gallbladder folded on itself

2. Gallbladder fold mimics dilated bile duct.3. Sludge filled gallbladder looks like liver tissue.4. Agenesis.5. Duct stones with agenesis6. Gallbladder ectopia7. After cholecystoenterostomy, food and gas mimic stones.8. Fundal and Hartmann stones not noticed.

Diagnostic errors:1. Bouveret's syndrome called stone filled gallbladder.2. Cholecystoses (adenomyosis and cholesterolosis).3. Intramural gas called stones or cholecystosis.4. Porcelain gallbladder.5. Milk ofcalcium bile.6. Sludge called tumour, polyp or stone and vice versa.7. Gallbladder thickening called cholecystitis.8. Post-cholecystectomy scar and clips called disease.9. Food and gas called stones after cholecystoenterostomy.

10. Asymptomatic gallstones taken as cause of symptoms.11. Cancer not recognized or considered.

© The Fellowship of Postgraduate Medicine, 1987

Correspondence: E.J. Fitzgerald, M.B., M.R.C.P.I.,F.R.C.R.*Present address: Toronto General Hospital, 200 ElizabethStreet, Toronto, Ontario, Canada M5G 2C4Accepted: 16 December 1986

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526 E.J. FITZGERALD & A. TOI

use of equipment and performance of the ultrason-ographic examination. Anatomical problems relate tonormal anatomical variants as well as physiologicalchanges .in the gallbladder and bile which may bemisinterpreted as disease. Diagnostic problems relateto errors of interpretation of ultrasonographicappearances.

Technical problems

For elective studies, the patient should be fasted for 12hours to allow adequate gallbladder distension to aidthe examination and to prevent mistaking as abnor-mal, the normally thickened wall of the physio-logically contracted gallbladder.6

Incorrect identification of another organ (bowel,stomach, duodenum, aorta, ligamentus teres)7 as thegallbladder will cause errors. Only the meticulousidentification of landmarks such as the right portalvein and following the main lobar fissure to thegallbladder can avoid such errors. We have encoun-tered a case of an ovarian dermoid on a long pediclemigrating to the subhepatic fossa adjacent to thegallbladder. Torsion of the pedicle led to pain andtenderness typical of gallbladder disease. Ultrason-ographically, this mass mimicked cholecystitis, with'stones' and debris which shadowed and moved withalteration of patient position.Once the gallbladder has been located, the examiner

must choose transducers with a suitable focal range.The common transducers used for abdominal examin-ation (3.5 MHz long focus) often give poor, noise filledimages of the gallbladder which may lie only 2-3 cmfrom the skin. Such gallbladders are adequatelyexamined only with smaller crystal transducers ofhigher frequency (e.g. 5 MHz) having a focal zone atthe gallbladder depth. We do not hesitate to employhigh frequency linear array scanners if the gallbladderis very superficial and obscured in the main beam noisezone of the sector equipment. Alternatively with suchsuperficial gallbladders, a standoff device may be usedor the liver itself may be employed as a standoff toplace the gallbladder within the focal zone of thetransducer.The absence of a distal acoustic shadow reduces the

probability of an echo being a gallstone from 100% to61 %.'° All gallstones should cast shadows irrespectiveof size or composition." The demonstration of suchshadows is entirely dependent on an appropriatelynarrow beam profile, as determined by transducerselection and machine settings. Ifthe calculus can stopenough of the beam to prevent sound transmissionbeyond it, shadowing will occur (Figure 1).The characteristics of the 'shadow' have also been

utilized. A calculus' shadow is said to be 'clean' andsharply defined. This is contrasted to the indistinctlymarginated and reverberation echo filled 'shadow'

Figure 1 Stones and polyp (arrow) in the gallbladder.Note the clear shadowing behind the calculi and theabsence of shadow behind the polyp.

associated with intestinal gas.'2"3 We have found thisto be a difficult sign to employ with confidence.

Failure to move the patient during the examinationis another source of error. Gallstones are diagnosedmost confidently if they can be shown to move duringthe examination by having the patient assume adecubitus or erect position.'0 We have all too frequen-tly seen stones for the first time when they moved asthe patient changed position (Figures 2a and b).

Artifactual side lobe echoes from adjacent struc-tures are frequently written into the gallbladder lumenwhere they can be mistaken for sludge or calculi.'4Such spurious echoes are not constant as the trans-ducer or patient are moved. The operator needs to befamiliar with the artifactual echoes peculiar to his/herequipment.

There are some patients whose habitus will defeatthe most skilled examiner. In such cases we recom-mend further gallbladder evaluation with alternativeimaging techniques.

Anatomical and physiological variants

Several normal anatomical structures and variants in,and about, the gallbladder have been mistaken fordisease. Similarly, varying normal physiological statesmay create problems.

Folds are frequently present in the gallbladder.They cause confusing echoes and they may castshadows.'5 The junctional fold at the junction of thebody and infundibulum of the gallbladder and thefolds of the valves of Heister are a common source of

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ULTRASOUND AND GALLBLADDER DISEASE 527

Figure 3 A kink in the hepatic artery near the neck ofthegallbladder creates a strong specular echo and shadowwhich mimic a calculus in the gallbladder neck. Views inother directions and Doppler assessment revealed its trueidentity. Note also that the adjacent gallbladder is filledwith sludge and virtually isoechoic with the liver. It isrecognized only through identification of the subtlegallbladder-liver interface line (arrows).

Figure 2 (a) The multiple gallstones layered on thedependent gallbladder wall are difficult to detect asmachine gains are too high and transducer focus is toodeep. (b) the calculi become easily visible when the patientis moved and the stones float free. Also, gains have nowbeen set appropriately.

confusion. It has been suggested that if shadowing isseen from the region of the neck of the gallbladder inthe absence of dilation of the organ, then one shouldregard the shadowing with suspicion.'6 Such shadow-ing may result from sound attenuation and reflectionby folds or from refractive effects seen in any areawhere fluid and solid interfaces coexist' (Figure 3).

Similarly, a long narrow gallbladder folded back onitselfmay produce a 'septum' parallel to the long axisof the gallbladder. This may produce echoes whichhave been mistaken for stones.'8 A similar redundant

or folded neck of gallbladder may mimic a dilatedcommon bile duct.'9

Failure to demonstrate a physiologically distendedgallbladder in a fasting patient is reported to indicate adiseased gallbladder.'0"2 In our experience, it is veryrare not to be able to locate an even minute, contrac-ted, diseased gallbladder if correct transducers andtechniques are employed. We have, however, encoun-tered gallbladders which are distended with echogenicbile that is iso-echoic with liver. This renders thegallbladder invisible until the specular echo of its wallbecomes visible or a small pocket of non-echogenicbile is identified (Figure 3). Gallbladder agenesis is anuncommon condition occurring in only 1/2500 to1/5000 patients.' It is a diagnosis of exclusion whichshould be entertained only if the gallbladder fossa isclearly visible and shown not to contain the gallblad-der and all sites of gallbladder ectopia have beenassessed. These include the abdominal wall, beneaththe left lobe of the liver or retroperitoneally.2' Whilegallbladder agenesis is rare, it does not result inimmunity from cholelithiasis, since gallstones mayform in the bile ducts of patients lacking a gallblad-der.?"Food' or air,23 may enter the gallbladder and bile

ducts after surgical or spontaneous connections ofeither the gallbladder or bile ducts to bowel. Suchechoes can be mistaken for calculi if the appropriatehistory is not available. A radiograph of the gallblad-

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der area may confirm the presence of gas, but in ourexperience, ultrasonography is more sensitive in detec-ting such small gas collections. In such cases, theexaminer may be able to differentiate the less distinctechoes arising from gas as opposed to calculi'3 to reachthe correct diagnosis (Figure 4).The specific gravity of bile may exceed that of

gallstones and cause them to float. Stones may thus beoverlooked as they lie in the reverberation echo fillednon-dependent part ofthe gallbladder. Recognition ofthe characteristic shadow may be the only clue whichleads to demonstration of such calculi. Bile specificgravity is increased by oral cholecystographic agents24and floating stones should be considered if suchstudies have been recently performed. However,Carroll25 demonstrated that floating could occur with-out prior contrast administration (Figures 5a and 5b).Stones which contain gas,26 gas and calcium27 and purecholesterol stones22 float in normal bile. As gas-containing calculi also float, this sign cannot be usedas an indication for chemotherapeutic treatment,despite the recommendation to do this.28The fundus and neck of the gallbladder are subop-

timally examined by ultrasound. We have missed evenlarge calculi of several centimetres impacted in boththe fundus and in Hartmann's pouch. In the fundus,such stones are generally impacted behind a 'waist' inthe gallbladder, possibly due to adenomyomatosis.Because the fluid bile pocket appears to close towardthe fundus, one tends to overlook the stone in the non-bile-filled fundal pouch which has the appearance ofadjacent colon. It is likely that at ultrasonography, wecommonly miss the small fundal thickened patch ofadenomyomatosis which was easily recognized at oralcholecystography by the characteristic Rokintansky-Aschoff sinuses (Figures 6a and b). Similarly, in asteeply angled gallbladder, stones in Hartmann'spouch can be difficult to discriminate from the normal

Figure 4 Air bubbles with emphysematous cholecystitismimic floating stones.

Figure 5 (a) Floating calculi in patient not associatedwith oral cholecystographic opacification. (b) Reverbera-tion echoes mimic floating gallstones.

echogenic valves of Heister, portal structures andadjacent duodenum. Also, the gallbladder may notalways be totally included in a single axial ultrasoundimage. The entire organ must be scanned meticulouslyin at least two planes to ensure that all parts have beenseen, so that such errors may be obviated.

Diagnostic errors

Thickening of the gallbladder wall to 3 mm or morehas been shown to be a non-specific sign which may bepresent in many disorders of the gallbladder, as aresponse of the normal gallbladder to disease else-where (e.g. hypoproteinaemia, heart failure) and evenin the normal patient with physiological contraction ofthe gallbladder.29 It should not be taken as a definitivesign ofcholecystitis in the absence ofother corroborat-ing signs. Acute cholecystitis is not always associatedwith ultrasonographically detectable thickening of thegallbladder wall. This should be remembered in thesick, debilitated or post-operative patient in whomacalculous cholecystitis is sought. Wall thickening

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Figure 6 (a) Subtle thickening at the gallbladder fundus(arrow). This area of the gallbladder is frequently poorlyassessed at ultrasonography. (b) Fundal aden-omyomatosis shown by oral cholecystography.

may be detected in only about 2/3 patients with thiscondition.30

Bile is rendered echogenic by the presence ofcalcium bilirubinate and cholesterol crystals.' Suchechogenic bile or sludge is commonly seen in thegallbladder of debilitated, fasting or intravenously fedpatients. The sludge can be quite viscid and movementunder gravity may be very slow or absent. If nomovement is demonstrated then the picture maymimic a sessile gallbladder tumour.312 A repeat examin-ation after regular meals have been resumed will allowthe correct diagnosis. The presence of sludge does notexclude calculi which can be detected as echogenic,shadowing foci in the sludge. Simple sludge is gen-erally homogenous and of uniform echogenicity. Onoccasion, sludge may coalesce as 'sludge balls' or'tumefactive sludge'. These should not be mistaken for

Figure 7 Patient on intravenous feeds whose gallbladdercontains a sludge case and echogenic 'sludge balls' whichdo not shadow. These cleared spontaneously after returnto normal diet. The visible shadow results from gas in theduodenum and should not be misinterpreted to arise fromthe contents of the gallbladder.

polyps or stones (Figure 7). After gallbladder stimula-tion, they should disappear.The wall-echo-shadow (WES) triad33 or double-arc-

shadow34 has been felt to be characteristic for gall-stones within a contracted gallbladder. Recently a caseof Bouveret's syndrome or gallstone ileus mimickingthis sign has been reported.35 The falsely positive WESsign resulted from imaging the perforated gallstoneinside bowel lumen. This is an extremely rare condi-tion but it should be considered especially in womenaged over sixty who complain of upper intestinalobstruction in addition to gallbladder symptoms.

Several other disorders can give rise to appearancessimilar to theWES triad, namely porcelain gallbladder(Figures 8a and b),36 emphysematous gallbladder, milk.of calcium bile37 or gallbladder wall microabscesses.3"Thus careful attention should be given to clearlyidentifying the features of the WES triad so that theseother potentially more clinically significant conditionswill not be overlooked. If this triad cannot be demon-strated with confidence, then a plain film of theabdomen or computed tomography may be necessary.If porcelain gallbladder is suspected, then furtherinvestigation of both the gallbladder for malignancyand the liver for metastases is indicated since there is a22% incidence of gallbladder malignancy in thiscondition.39When echoes and shadows without definite

evidence of a gallbladder wall are seen, careful atten-

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Figure 8 (a) Stone-like shadow in the gallbladder fossasuggesting the wall-echo-shadow complex of cholelith-iasis. (b) Computed tomographic scan reveals that theshadowing results from mural calcification in this patientwith porcelain gallbladder who has no calculi.

tion must be paid to the site of origin of the echoes.Adenomyomatosis with stones in the gallbladderwall can give this appearance. Intramural gas may givea similar appearance, but the presence of typical gasreverberation behind the echoes may help to differen-tiate this from calculi.' However, in the presence of afluid-filled gallbladder such intramural gas may beconfused with gas in the bowel. In the case ofintramural gas, a shift in position of the patientproduces a gravity-induced equivalent shift ofintramural and intraluminal gas, thus helping toconfirm the diagnosis.4' Indeed, a definitive diagnosisofemphysematous cholecystitis cannot be made with-out the aid of radiological studies.4'The post-cholecystectomy gallbladder fossa can

present confusing appearances. A history of cholecys-tectomy may not be elicited in patients who may have

forgotten the procedure or in whom cholecystectomywas incidental to surgery being carried out for otherreasons. After gallbladder removal, strong echoes withacoustic shadowing may arise from the region of thegallbladder bed.42 In the absence of surgical clipswhich can cause this appearance43 it is assumed thatscar collagen gives rise to these findings. Some patientshave undergone surgery on the basis of thisappearance.42 The surgical removal of the gallbladdermay be confirmed with a simple radiograph showingthe presence of clips, but if necessary, other investiga-tions such as endoscopic retrograde cholangiographycan be undertaken.

Gallbladder cancer is not uncommonly first diag-nosed at autopsy. This results from its rarity, vaguesymptomatology, difficulty of diagnosis and, notinfrequently, from simply not considering it as adiagnostic possibility. Ultrasonographically, it can beeasily missed for several reasons. It is commonly(80%) accompanied by calculi and one forgets to lookbeyond the initial findings. The mass may be echo-poor and appear fluid-like unless gain is increased.The echoes may be interpreted as sludge. We havemissed a 10cm infiltrating mass hanging from thefundus ofthe gallbladder simply because we examinedonly the gallbladder with real time equipment and didnot appreciate the mass which extended moreinferiorly and mixed into bowel and omental echoes.One needs to remember that asymptomatic gall-

stones are common and that other conditions havesymptoms similar to those ofthe diseased gallbladder.4Indeed, acute cholecystitis is confirmed in fewer than50% of patients in whom it is clinically diagnosed.45Ultrasonography, unlike cholecystography, allows theentire right upper quadrant to be evaluated fordiseases in other organs which may be the source ofthepatient's symptoms. We stress that a request forultrasonographic gallbladder assessment really entailsexamination of the entire upper abdomen and shouldnot be confined to the gallbladder.

Conclusions

Ultrasonography provides a rapid and accuratemethod of evaluating the gallbladder and right upperquadrant for disease. As experience with the techniquegrows, we are becoming aware of pitfalls which willtrap the unwary and give rise to both false positive andfalse negative studies. Sound anatomical knowledge,adherence to optimal technique, strict diagnosticcriteria .and knowledge of the pitfalls are necessary toavoid diagnostic inaccuracy and potential patientharm. One should not hesitate to use other diagnosticmodalities when there is diagnostic uncertainty or ifconfirmation of the findings is important.

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