ceus in abdominal trauma: multi-center study

CEUS in abdominal trauma: multi-center study

Orlando Catalano,1,2 Luca Aiani,3 Libero Barozzi,4 Daniela Bokor,5 Armanda De Marchi,6

Carlo Faletti,6 Fabio Maggioni,5 Nicola Montanari,7 Paolo Emilio Orlandi,7 Alfredo Siani,1

Paul S. Sidhu,8 Peter K. Thompson,9 Massimo Valentino,4 Angelo Ziosi,4

Alberto Martegani3

1Department of Radiology, I.N.T. Pascale, via Semmola, 80131 Naples, Italy2via Crispi 92, 80121 Naples, Italy3Department of Radiology, Valduce Hospital, Como, Italy4Department of Emergency Radiology, S.Orsola-Malpighi Hospital, via Massarenti 9, 40138, Bologna, Italy5Imaging Guided & Integrated Technology Department, Bracco Imaging SpA, Milan, Italy6Department of Radiology, C.T.O., Turin, Italy7Department of Radiology, Maggiore Hospital, Bologna, Italy8Department of Radiology, King’s College Hospital, Denmark Hill, London SE5 9RS, UK9Department of Accident and Emergency, College Hospital, Denmark Hill, London SE5 9RS, UK

Abstract

The objective of this study was to evaluate the concor-dance of US and contrast-enhanced US (CEUS) with CTin the assessment of solid organ injury following blunttrauma. Patients underwent complete US examination,including free fluid search and solid organ analysis.CEUS followed, using low-mechanical index techniquesand SonoVue. CT was performed within 1 h. Among 156enrolled patients, 91 had one or more abnormalities(n = 107) at CT: 26 renal, 38 liver, 43 spleen. Sensitivity,specificity, and accuracy for renal trauma at baseline USwere 36%, 98%, and 88%, respectively, after CEUS val-ues increased to 69%, 99%, and 94%. For liver baselineUS values were 68%, 97%, and 90%; after CEUS were84%, 99%, and 96%. For spleen, results were 77%, 96%,and 91% at baseline US and 93%, 99%, and 97% afterCEUS. Per patient evaluation gave the following resultsin terms of sensitivity, specificity and accuracy: 79%,82%, 80% at baseline US; 94%, 89%, and 92% followingCEUS. CEUS is more sensitive than US in the detectionof solid organ injury, potentially reducing the need forfurther imaging. False negatives from CEUS are due tominor injuries, without relevant consequences for patientmanagement and prognosis.

Key words: Abdomen trauma—Liver trauma—Spleentrauma—Kidney trauma—Traumasonography—Sonography contrast media

In most European and Asian-Pacific countries, ultra-sound (US) is used as the initial tool to screen patientswith suspected blunt abdominal trauma, both in iso-lated abdominal trauma or in the polytrauma victim[1]. In the United States the usefulness of US in thecontext of abdominal trauma has been much under-valued; trauma imaging was mainly based on contrast-enhanced computed tomography (CT) imaging, withvery high rates of true negative results and the relatedradiobiological and pharmacological invasiveness [1].In the last decade, American authors have discoveredthe US, although mainly in the modality called focusedassessment with sonography for trauma (FAST) [2–5].FAST is now established as a peritoneal fluid-targeted,emergency physician-performed tool that is usedworldwide for the initial work-up of trauma victims.FAST is a minimized technique, whose practical valueparticularly in the stable patient remains unproven. Inour institutions we use a ‘‘full potential’’ US technique,eventually including the selective use of IV contrastmedium.

A multi-centric, international, prospective study wasconducted to compare the performance of continuous-mode, contrast-enhanced US (CEUS) with CT in sub-jects with abdominal trauma.Correspondence to: Orlando Catalano; email: [email protected]

ª Springer Science+Business Media, LLC 2008

Published online: 6 August 2008AbdominalImaging

Abdom Imaging (2009) 34:225–234

DOI: 10.1007/s00261-008-9452-0

Materials and methods

Study design

This study was designed as a prospective, open label,European, multi-center trial involving six centers. Onehundred and fifty patients presenting acutely with ahistory of blunt abdominal trauma were enrolled. Theobjective of the study was to compare the performance ofconventional B-mode US examination and the sonoVue-contrast-enhanced US with CT in the detection/exclusionof post-traumatic abdominal injuries.

On arrival, all patients underwent the following se-quence of examinations: conventional (fundamental) USimaging, contrast-enhanced US, and (whenever possible)contrast-enhanced CT. The same radiologist performedbaseline and enhanced US while another, blinded, radi-ologist evaluated the CT scans. Both radiologists inde-pendently completed their study charts.

Patients

Each institutional ethic review board approved the studyand all centers used the same forms. Inclusion criteriawere: age older than 14 years, clinical and laboratorysuspicion of blunt or penetrating abdominal trauma,availability of US, CEUS, and CT study performedwithin 1 h, availability of a reference standard (CT orsurgery). The study enrolled 156 patients.

The revised trauma score (RTS) and the injuriesseverity score (ISS) were calculated. RTS was obtainedconsidering: 0.9368 9 Glasgow Coma Scale score +0.7326 9 systolic blood pressure + 0.2908 9 respira-tory rate. ISS is an anatomical scoring system that pro-vides an overall score for patients with multiple injuries.Each injury is assigned an abbreviated injury scale scoreand is allocated to one of six body regions (head, face,chest, abdomen, extremities including pelvis, external).

Baseline US technique

In all cases, a rapid but complete survey of all abdominalparenchymas and abdomino-pelvic spaces was obtainedby using conventional gray-scale US imaging. Carefulsearch for peritoneal fluid, retroperitoneal fluid, and or-gan injury was carried out. These baseline studies wereperformed by radiologists experienced with US, using thefollowing scanners: EsaTune (Esaote, Italy), Technos(Esaote, Italy), or ATL HDI 5000 (Philips, The Neth-erlands).

Phased-array transducers (2–6 MHz) were em-ployed. In selected cases, the operator additionallyemployed high frequency probes (5.5–10 MHz), power-Doppler imaging mode, and/or tissue harmonic imagingmode to maximize diagnostic effectiveness of unen-hanced US.

CEUS technique

CEUS studies were carried out with the harmonic, low-mechanical index, contrast-specific softwares contrasttuned imaging (CnTI) and pulse inversion.

CEUS was always performed immediately after thebaseline US, using a 2.5 or a 3.5 MHz transducer and alow acoustic power setting (mechanical index, 0.05–0.1).A single focus was placed deep to the area of interest;general gain was set low, below noise threshold with themost superficial step of the time-gain compensationcurve minimized. Amplification was set to minimum, torecognize, at the moment of contrast medium arrival,only the most echoic interfaces (such as diaphragm,vessels wall, and gallbladder wall).

We employed the ‘‘second-generation’’ contrastmedium SonoVue (Bracco, Milan, Italy). SonoVue con-sists of microbubbles containing an inert gas (sulfurhexafluoride) and covered by a stabilizing phospholipidicmembrane [6, 7]. The reconstituted product provides8 lL/mL of SF6 microbubbles. SonoVue volume(4.8 mL) was fractionated into two 2.4-mL doses eachinjected as a quick bolus through an antecubital vein anda 18–20G catheter followed by 5–10 mL normal saline(0.9% NaCl) flush through a three-way stopcock.Immediately after the first contrast medium injection, theright-sided organs (the right kidney and, possibly, adre-nal first and the liver subsequently) were explored for 1–3 min. Thereafter, the second SonoVue dose wasadministered, focusing on left side organs (the left kidneyand, possibly, adrenal first, the pancreas, and finally thespleen) for other 3–4 min.

At the moment of injection a timer was initiated onthe US scanner and a continuous video recording of theexamination was commenced. Periodically (e.g., 3–4 times/exam) a high power flash could be supplementedto the continuous acquisition, briefly rupturing micro-bubbles within insonated volume allowing a kind oftransient opacification resetting (reperfusion evaluation).In addition, the operator could revert to baseline USmode (now set at a low-mechanical index to avoid mi-crobubbles disruption) to re-examine the area of interestand return to contrast mode as needed.

Standard of reference

Standard of reference for this study was CT and/orsurgery. CT was performed in 151 out of 156 patients,within 1 h following baseline US and CEUS. In fivesubjects CT was not performed as a consequence of pa-tient instability and the need for prompt surgery. Surgerywas necessary in 23 patients with the remaining subjectstreated conservatively. Three patients also underwentangiographic assessment.

Radiologists experienced with emergency helical CTimaging interpreted the CT studies. Most exams were

226 O. Catalano et al.: CEUS in abdominal trauma

performed with single-detector scanners with 0.75–1 srevolution time and included the following: SomatomPlus 4 system (Siemens AG, Germany), Emotion system(Siemens), PQ6000 system (Picker International, USA),and LightSpeed Ultra system (GE Healthcare, USA). ASensation 16-row tomograph (Siemens) was also em-ployed.

No patient received oral contrast medium and mostpatients had a pre-contrast acquisition series. The con-trast-enhanced study was carried out using 5- or 8-mmcollimation, 5 or 7.5-mm/s table speed, 120 kVp, 5-mmreconstruction interval. A non-ionic contrast medium(iomeprol 350 mgI/mL, Iomeron, Bracco-iopamidol300 mgI/mL, Iopamiro, Bracco-iohexol 350 mgI/mL,Omnipaque, Amersham Health) was administered via18–20 G angiocatheter and power injector. A volume of100–150 mL was injected at 2–4 mL/s. When a two-phase technique was employed, delay ranged from 40 to50 s for the first contrast-enhanced acquisition and from80 to 120 s for the second acquisition. Patient undergo-ing single-phase acquisition were scanned at 60–90 sfrom contrast injection (2 mL/s).

Data collection and statistical analysis

Statistical analysis of the data was performed with thestatistical analysis software (SAS) ver. 8.2 for WindowsSystem.

Efficacy evaluation was done on site by the investi-gators who evaluate the presence/absence of abdominallesions with baseline US and CEUS. The standard ofreference was CT and/or surgery.

The following definitions were used to calculate theprimary endpoints. True positive was defined as presenceof abdominal lesion based on both ultrasonography andthe truth standard. True negative was defined as absenceof abdominal lesion based on both US and the truthstandard. Sensitivity was defined as the number of truepositives divided by number of abdominal lesions basedon the standard of reference. Specificity was defined asthe number of true negatives divided by the number ofabsences of abdominal lesion based on the truth stan-dard. Accuracy was defined as the number of true neg-atives plus the number of true positives divided by thenumber of subjects examined with the truth standard.Positive predictive value was defined as the number oftrue positives divided by the number false positives plusthe number of true positives. Negative predictive valuewas defined as the number of true negatives divided bythe number true negatives plus the number of falsenegatives.

For comparison of the accuracy in diagnosis betweenthe techniques studied, the McNemar test was applied. AP value of less than 0.05 was considered to indicate astatistically significant difference.

Results

There were 118 male subjects (76%) and 38 females(24%). Mean age was 39 years, with a standard deviation±17 years and a range of 15–90 years.

The following RTS values were found in our 156patients: 1.96 (n = 2), 4.74, (n = 1), 5.05–5.96 (n = 9),6.09 (n = 24), and 7.20–7.84 (n = 120). Hence, RTSranged from 1.96 to 7.84.

The following ISS values were calculated: 0–10(n = 58), 11–20 (n = 63), 21–30 (n = 22), 31–40(n = 10), and 41–50 (n = 3). Consequently, ISS rangedfrom 0 to 50.

Sixty-five subjects had no abdominal abnormality and91 had one or more abnormality (total number of inju-ries = 107) at CT (or surgery) with the following dis-tribution: 26 renal, 38 liver, 43 spleen (Figs. 1–4). Twelvepatients had two abdominal injuries and one had threeinjuries.

At baseline US the distribution of abnormalitieswas: 12 renal, 29 liver, 37 spleen. Following CEUS the

Fig. 1. Liver trauma. (A) CEUS detects a complex hepaticlaceration (arrows). (B) CT demonstrates a very similarmorphology of injury (arrows).

O. Catalano et al.: CEUS in abdominal trauma 227

distribution was: 19 renal, 33 liver, 41 spleen. Theefficacy results for each organ are listed in Tables 1, 2,and 3.

Statistically significant difference was noted be-tween US and CT as for liver injury (P = 0.02) andkidney injury (P = 0.004), while difference did not

Fig. 2. Spleen trauma. (A) Unenhanced US shows subtle, ill-defined inhomogeneity of splenic parenchyma (arrows). (B) CEUSclearly demonstrates multiple lacerations (arrows). (C) Optimal CT correlation. (D) Optimal surgical correlation.


reach statistical significance as for spleen injury(P = 0.12).

Difference between CEUS and CT was not statisti-cally significant as for liver injury (P = 0.08) and spleeninjury (P = 0.25), while difference reached statisticalsignificance as for spleen injury (P = 0.045).

Overall accuracy of baseline US and CEUS wasconsidered combining the detection rate of organ injury

Fig. 4. Kidney trauma. (A) CEUS shows lack of right kidneyenhancement (arrows). Liver (L). (B) CT confirms renal totalnon-perfusion.

Table 1. Presence/absence of parenchymal lesion in liver using US,CEUS, and reference methods

Reference methods US CEUS

Total number of patients 156 156 156Patients with lesion 38 29 33Patients without lesions 117 127 123Indeterminate 1 0 0

Table 2. Presence/absence of parenchymal lesion in spleen using US,CEUS, and reference methods



Fig. 3. Spleen trauma. (A) Unenhanced US only detectsperisplenic hematoma (arrow). (B) CEUS additionally dem-onstrates a small parenchymal laceration (arrow). (C) Optimal

CT correlation, with evidence of both hematoma (black arrow)and laceration (white arrow).

Table 3. Presence/absence of parenchymal lesions in kidneys using US,CEUS, and reference methods




and the detection rate of peritoneal or retroperitonealfluid. Baseline US was true negative in 47 out of 156cases, true positive in 78, false negative in 21, and falsepositive in 10; hence, sensitivity was 79%, specificity 82%,accuracy 80%, positive predictive value 89%, and nega-tive predictive value 69%.

CEUS was true negative in 51 out of 156 cases, truepositive in 93, false negative in 6, and false positive in 6;consequently, sensitivity was 94%, specificity 89%,accuracy 92%, positive predictive value 94%, and nega-tive predictive value 89%.

A definite or possible diagnosis was reached in 83,138, and 149/156 patients undergoing baseline US,CEUS, or CT, respectively. CEUS only missed minortraumatic injuries. None of the patients with a CEUSexamination, which failed to identify an organ injury,required surgery or died as a consequence of ‘‘missed’’traumatic lesion. One patient died during surgery as aconsequence of intraperitoneal and retroperitonealbleeding following pancreatic laceration and portal veinavulsion; in this patient baseline US, CEUS, and CTdetected a large amount of hemoperitoneum and pan-creatic recess hematoma without clear depiction of pan-creatic injury.

Accuracy results for injury detection (aside consid-ering hemoperitoneum detection) are given in Tables 4,5, and 6. One patient showed a subtle hyperechoic areawithin the liver at baseline US, suggesting a possibletraumatic hepatic injury. CEUS and CT demonstrated ahypervascularized focal lesion (proved adenoma) in thispatient. Two patients had baseline US evidence of a

possible thin subcapsular hematoma of the kidney, sub-sequently demonstrated as absent at both CEUS and CTevaluation. In one patient baseline US and CEUS werenegative for injury with CT demonstrating a possible leftdiaphragmatic traumatic herniation; subsequent surgeryfound this to be probably non-traumatic.

Discussion

US, both as a complete survey or as a rapid, fluid-pointedassessment, is being used with increasing frequency inblunt abdominal trauma [8–12]. Nevertheless CT remainsthe most accurate and panoramic imaging tool in theassessment of trauma victims, with US proven effectivetool, at least in selecting patients that are candidates toCT. One of the main limitations of US, and the weakestaspect of FAST (by definition), is the low sensitivity fordirect demonstration of organ injury [13–18]. This is animportant drawback, especially in the subset of patientswhere parenchymal trauma is not combined with freefluid [19–22]. Peritoneal fluid is only an indirect sign oftrauma, on occasion being unrelated to trauma itself(ovulation, ascites, peritoneal lavage) [22]. Additionally,in some published series, organ injury without hemoper-itoneum was relatively common and was occasionallyfound in patients with severe injury degree, requiringsurgery or transcatheter embolization [20, 23]

In an effort to improve US sensitivity, several tech-nical aspects may be considered. High-resolution(>7.5 MHz) transducers may help recognizing minimalfluid collection or subtle parenchymal lesions in pediatricor slim adult subjects [24]. Tissue harmonic imaging ismore effective than fundamental US mode in recognizingfree fluid and in assessing abdominal organs for injurydetection [25, 26]. Catheter bladder distension may helpdetecting minimal amount of pelvic fluid [8, 10]. Color-and power-Doppler techniques can identify vasculariza-tion defects as a direct signs of parenchymal injury [27].Finally, injection of contrast medium, especially if com-bined with real-time, low-mechanical index technique,may improve detection and severity assessment ofabdominal injuries [17, 18, 28–31]. Judicious, patient-tailored use of all the above-mentioned options can boostUS capability.

Table 4. Accuracy for liver trauma detection

US CEUS

True negative 115 117True positive 26 32False negative 12 6False positive 3 1Total 156 156Sensitivity 68% 84%Specificity 97% 99%Accuracy 90% 96%Positive predictive value 90% 97%Negative predictive value 91% 95%

Table 5. Accuracy for spleen trauma detection

US CEUS


Table 6. Accuracy for kidney trauma detection

US CEUS



In this multi-institutional, prospective study we haveanalyzed the potential additional value of CEUS in pa-tients with abdominal trauma. To our knowledge this isthe largest series of patients with abdominal injuriesevaluated by using this imaging modality. Real-timeCEUS can directly demonstrate parenchymal injuries,appearing as non-enhancing defects within the enhancednormal tissue [17, 18, 28, 29]. Traumatic lesions appearsimilarly in different organs. Contusion, which appearsas areas of hypoechogenicity, becomes clearer as thesurrounding parenchyma is progressively enhanced.Laceration appears as clear hypoechoic linear deficien-cies or bands, usually oriented perpendicularly with re-spect to organ surface. Hematoma appears as non-enhancing area. CEUS depicts better than baseline USthe full extent of injury and eventual extent to organcapsule [17, 18, 28, 29]. CEUS can additionally detectfindings unrecognizable with conventional US, such asinfarcts and contrast extravasation. As is documented inthe CT literature [32–34], recognition of contrast mediumextravasation is very important since it indicates thepresence of on-going hemorrhage and need for invasivetreatment. Early experimental studies have demonstratedhow CEUS can detect contrast leakage as a sign of injury[35, 36], with subsequent articles reporting CEUSdetection of contrast extravasation in trauma patients[28, 29, 37]. In our series contrast extravasation wasrecognized in seven cases, all confirmed with CT (Fig. 5).

Contrast enhancement of abdominal parenchymaslasts long enough (up to 4–5 min) to allow adequateexploration of all organs. To optimize CEUS effective-ness, we employed two contrast medium injection, frac-tionating the 4.8 mL SonoVue dose into 2 injections.This allowed for assessment of each organ at the peak ofcontrast enhancement. Kidneys were studied immedi-ately after contrast medium injection as they have anintense opacification with a rapid wash-in and a rapidwashout. The liver was explored at an intermediate delayfrom injection because of its predominately portal-ve-nous blood supply. Finally the spleen was examined lastas this organ has the most prolonged opacification,whereas it demonstrates an inhomogeneous early phaseenhancement possibly causing misinterpretation. Inclinical practice a single 2.4 or 4.8 mL injection may alsobe sufficient to explore all organs, starting with the kid-neys and ending with the spleen [17, 18, 37]. The exam-iner frequently knows or ‘‘feels’’ from baseline USimaging, the organ or organs most probably injured andcan focus most of the CEUS study on the suspected area.Lastly, although this did not occur in our study, theSonoVue injection can be repeated.

Real-time CEUS exploration allows dynamic imagingof all changes, including findings unrecognizable withbaseline US such as active hemorrhage (contrastextravasation) [38]. A multi-planar, assessment allowedby CEUS permits examination of the whole course of

parenchymal lacerations. Additionally, the entire study isusually recorded during acquisition as a videoclip andthis allows revision of the study while the attendingmedical team actively manages the patient. Not infre-quently, in clinical practice, revision of the recordedstudy reveals details that were not noted during scanacquisition.

The European Federation of Societies for Ultrasoundin Medicine and Biology guidelines has recently listed thepotential applications of CEUS. ‘‘CT not available or

Fig. 5. Liver trauma. (A) CEUS shows multiple hepatic lac-erations (black arrows) with intraparenchymal contrast med-ium leakage (white arrow). Gallbladder (G). (B) CT confirmshepatic lacerations (black arrows) and contrast extravasation(white arrow).


contra-indicated, patient requires resuscitation beforeCT, CT is inconclusive or associated with artifacts,monitoring of known traumatic lesions, minor blunttrauma especially in children’’ [39]. These guidelines referto the liver but can be extended to other abdominal pa-renchymas.

In our experience CEUS is especially useful whenthe baseline US detects peritoneal/retroperitoneal fluidbut fails to identify organ injury and/or demonstratessubtle parenchyma changes. In addition patients posi-tive at baseline US may be examined in greater detail,allowing recognition of perfusion alterations such asparenchymal infarcts or contrast extravasation, notnormally demonstrated with conventional US. More-over, a negative US with persistent laboratory suspicion(unexplained anemia, deranged liver function test, ormicrohematuria) may be followed by CEUS. Clearly, inmany of these subjects, with US positive for fluid or forboth injury and fluid, CT should be performed insteadof CEUS.

CT is the most effective and panoramic modality intrauma victim imaging, with a mean room time that issimilar to that of US plus CEUS [28, 29]. Additionally, inmany trauma centers, CT scanners are now been placedinside the emergency room itself, minimizing patienttransport. Nevertheless, in our opinion CEUS may playa role in several clinical scenarios, such as imaging thestill unstable trauma patient, bed-side examination, iso-lated moderate-energy abdominal or flank trauma (sportor horse-riding accidents, falls, minor bicycle accidents),emergency room assessment (in selected cases), contrast-enhanced CT contra-indicated or failed or unclear, andmonitoring of conservatively treated injuries [17, 18].Not infrequently, emergent CT scans of trauma patientscan show motion or positioning artifacts and CEUS maybe used to better assess some unclear area or finding [17,18].

CEUS may allow further evaluation of subtle paren-chymal abnormalities shown by baseline US, to rule outinjury or to diagnose a non-traumatic change [17, 18]. Inour series one female subject with an inhomogeneouslyhyperechoic area within the liver was shown to bear ahypervascular, benign focal lesion after CEUS and CT(subsequently proven adenoma). Operator confidence inaffirming or in excluding the presence of a traumaticinjury is certainly boosted by CEUS. A larger use ofCEUS may allow to reduce observation time for patientsnegative at baseline US, decreasing the number of re-peated US examinations and expediting patient dis-charge. In the future CEUS may permit imaging ofpatients not ideal for contrast-enhanced CT such aschildren or pregnant women. Since our series demon-strates that US + CEUS allows confident exclusion ofsignificant abdominal injuries, many patients may bedischarged home, after a period of observation, withoutbeing submitted to CT.

Follow-up of non-operative abdominal traumatreatment is, in our opinion, the main forthcomingapplication of CEUS. To date, follow-up of trauma casestreated non-operatively has been performed with US orwith CT [40–45]. Choice of the imaging modality and ofthe appropriate timing for imaging studies is still de-bated. In our series follow-up studies were not includedand, to our knowledge, there are no reports on the cost-effectiveness of CEUS monitoring of abdominal injuries(apart from two anecdotal pediatric cases [30]). Never-theless, in patients where injury location has been iden-tified, use of CEUS may significantly decrease thenumber of follow-up CT examinations [17, 18]. As amatter of fact, CEUS may demonstrate all aspects rele-vant for monitorization: amount of peritoneal fluid, in-jury extent, distance from organ capsule, organ hilumand major vessels, and development of contrast extrav-asation or pseudoaneurysm.

US limitations such as obesity or difficulty inexploring deeply located areas are usually not improvedby contrast medium. In general CEUS should not beused to overcome these limitations. In addition, currentCEUS systems have some specific drawbacks, such asloss of spatial resolution and overall image quality anddifficulty in assessing deep regions such as right liver lobeposterior aspect (specially in patients with steatosis),subphrenic spleen parenchyma, and kidneys (specially infat subjects) [17, 18].

To date, only a limited number of articles on CEUSimaging for abdominal trauma have been published.Catalano et al. [28, 29] reported their experience onspleen trauma (18 positive cases) and on liver trauma (23positive cases). Miele et al. [46] published their study onliver trauma, with 31 positive cases included. Polettiet al. [37] reported their experience in 25 patients withCT-proven solid organ injury and false negative US. Kimet al. [47] included two trauma cases in their series onrenal perfusion abnormalities. Oldenburg et al. [30]illustrated two pediatric traumas recognized and moni-torized with CEUS. Thorelius [17, 18] published tworeview articles. A very recent paper [31] has also dem-onstrated the feasibility of a FAST examination per-formed with microbubble US contrast, by evaluatingsimulated patients. All these authors (and their data),with the exception of Poletti et al. [37], agree on therelevant opportunities offered by CEUS for bluntabdominal trauma imaging.

Poletti [37] showed a limited sensitivity for USdetection of parenchymal injuries and a good but stillunsatisfactory sensitivity of CEUS. On a per lesion basis,sensitivity was 40% for admission US, 57% for controlUS, and 80% for CEUS. On a per patient basis, sensi-tivity was 45% for admission US, 65% for control US,and 83% for CEUS. CEUS missed 14 injuries, includingfour major injuries in four patients. Some aspects mayexplain the differences between our data and those from


Poletti et al. First, we employed a real-time, ultralowmechanical index technique while Poletti employed apulse inversion mode with medium level mechanical in-dex (0.18). Second, the overall number of CEUS studiesin Poletti’s series and the number of positive CEUSstudies was too limited to achieve adequate statisticanalysis (25 and 13, respectively). The 25 cases enrolledin Poletti’s study seem to be the first trauma patientsexplored with CEUS in their institution and conse-quently a learning curve artifact may have worsenedeffectiveness. Moreover, Poletti included the adrenals(and the related, predictable, low sensitivity of US andCEUS) among solid organs; we only considered majorparenchymas (i.e., liver, spleen, and kidney) as targets forretrospective analysis, since adrenal hematomas usuallydo not carry relevant consequences. Finally, the eventualpresence of peritoneal fluid in patients with organ inju-ries undetected by CEUS, and specially in those patientswith major injuries, is unclear in Poletti’s series: an US ora CEUS positive for free fluid only must be considered atleast a partial positive result, since it drives to furtherinvestigation. Aside from these considerations, Poletti’sresults are in line with our findings and with the pub-lished literature in the main aspects. First, in Poletti’sseries, CEUS improves admission US and even controlUS sensitivity. Second, almost all relevant cases weredetected with CEUS (100% of grade III–V spleen inju-ries, grade IV liver injuries, and grade III–V renal andadrenal injuries, and 88% grade III liver injuries in Po-letti’s series) and none of the CEUS false negative casesrequired surgery or embolization. Poletti and colleaguesconcluded that CEUS still misses some solid organinjuries and that consequently CEUS cannot replace CTin the triage of patients with negative admission US. Weagree that CT should not be replaced. However, CEUScan be selectively employed to initially screen these pa-tients and to decrease the number of cases submitted toCT. This may allow performing CT in those patients thatwould get benefit from this additional radiation andcontrast medium exposure.

Some intrinsic limitations of our study should also beconsidered. First, the number of positive cases for eachorgan is limited and more numerous reports are neededto definitively assess the effectiveness of CEUS. Second,in some of the institutions included in our multi-centricsurvey, experience with CEUS imaging for trauma wasinitially limited and consequently a learning curve hasprobably influenced the final CEUS statistics. A ‘‘learn-ing curve bias’’, due to unfamiliarity with contrastmedium and technique, involved some of the centersenrolled in our survey. In addition, for organizationreasons, we could not perform an off-site analysis ofenrolled cases and all data were based on evaluation ofin-site study reports. Also, radiologists performingCEUS were not blinded to US findings, since the sameradiologist performed CEUS immediately after US.

Conclusion

Our prospective study shows how CEUS is more sen-sitive than US and is almost as sensitive as CT in thedetection of solid organ injury in blunt abdominaltrauma. CEUS allows more accurate assessment of solidorgan lesions in comparison with baseline US. It ismore accurate and informative than conventional USand correlates better with CT findings. By using CEUSonly lower grade injuries, not associated with hemo-peritoneum, are missed, but these patients usually re-cover uneventfully. Contrast enhancement may allow toovercome some intrinsic limitations of US and conse-quently to increase its diagnostic role. Consequently,the number of CT studies, with their cost, contrastmedium-related risk, and radiation exposure can bedecreased.

Acknowledgment. Authors are in debt with Massimo Di Maio, M.D.,for providing statistical analysis.

References

1. Scaglione M (2004) The use of sonography versus computedtomography in the triage of blunt abdominal trauma: the Europeanperspective. Emerg Radiol 10:296–298

2. Shih H-C, Wen Y-S, Ko T-J, et al. (1999) Noninvasive evaluationof blunt abdominal trauma: prospective study using diagnosticalgorithms to minimize nontherapeutic laparotomy. World J Surg23:265–270

3. Dolich MO, McKenney MG, Varela JE, et al. (2001) 2,576 ultra-sounds for blunt abdominal trauma. J Trauma 50:108–112

4. McKenney KL, Nunez DB, McKenney MG, et al. (1998) Sonog-raphy as primary screening technique for blunt abdominal trauma:experience with 899 patients. AJR 170:979–985

5. Rothlin MA, Naef R, Amgwerd M, et al. (1993) Ultrasound inblunt abdominal and thoracic trauma. J Trauma 34:488–495

6. Bokor D, Chambers JB, Rees PJ, et al. (2001) Clinical safety ofSonoVue, a new contrast agent for ultrasound imaging, in healthyvolunteers and in patients with chronic obstructive pulmonarydisease. Invest Radiol 36:104–109

7. Morel DR, Schwieger I, Hohn L, et al. (2000) Human pharmaco-kinetics and safety evaluation of SonoVueTM, a new contrast agentfor ultrasound imaging. Invest Radiol 35:80–85

8. Brown MA, Casola G, Sirlin CB, et al. (2001) Blunt abdominaltrauma: screening US in 2,693 patients. Radiology 218:352–358

9. Richards JR, Knopf NA, Wang L, et al. (2002) Blunt abdominaltrauma in children: evaluation with emergency US. Radiology222:749–754

10. Sirlin CB, Brown MA, Andrade-Barreto OA, et al. (2004) Bluntabdominal trauma: clinical value of negative screening US scans.Radiology 230:661–668

11. Tas F, Ceran C, Atalar MH, et al. (2004) The efficacy of ultraso-nography in hemodynamically stable children with blunt abdomi-nal trauma: a prospective comparison with computed tomography.Eur J Radiol 51:91–96

12. Lingawi SS, Buckley AR (2000) Focused abdominal US in patientswith trauma. Radiology 217:426–429

13. Emery KH, McAneney CM, Racadio JM, et al. (2001) Absentperitoneal fluid on screening trauma ultrasonography in children: aprospective comparison with computed tomography. J Pediatr Surg36:565–569

14. Poletti P-A, Kinkel K, Vermeulen B, et al. (2003) Blunt abdominaltrauma: should US be used to detect both free fluid and organinjuries? Radiology 227:95–103

15. Poletti P-A, Wintermark M, Schnyder P, et al. (2002) Traumaticinjuries: role of imaging in the management of polytrauma victim(conservative expectation). Eur Radiol 12:969–978


16. Taylor GA, Sivit CJ (1995) Posttraumatic peritoneal fluid: is it areliable indicator of intraabdominal injury in children? J PediatrSurg 30:1644–1648

17. Thorelius L (2004) Contrast-enhanced ultrasound in trauma. EurRadiol 14(suppl 8):P43–P52

18. Thorelius L (2003) Contrast-enhanced ultrasound: beyond the liver.Eur Radiol 13:N91–N108

19. Chiu WC, Cushing BM, Rodriguez A, et al. (1997) Abdominalinjuries without hemoperitoneum: a potential limitation of fo-cused abdominal sonography for trauma (FAST). J Trauma42:617–623

20. Shanmuganathan K, Mirvis SE, Sherbourne CD, et al. (1999)Hemoperitoneum as the sole indicator of abdominal visceral inju-ries: a potential limitation for screening abdominal US for trauma.Radiology 212:423–430

21. Ochsner MG, Knudson MM, Pachter HL, et al. (2000) Significanceof minimal or no intraperitoneal fluid visible on CT scan associatedwith blunt liver and splenic injuries: a multicenter analysis. JTrauma 49:505–510

22. Yoshii H, Sato M, Yamamoto S, et al. (1998) Usefulness andlimitations of ultrasonography in the initial evaluation of bluntabdominal trauma. J Trauma 45:45–51

23. Poletti PA, Mirvis SE, Shanmuganathan K, et al. (2000) CT criteriafor management of blunt liver trauma: correlation with angio-graphic and surgical findings. Radiology 216:418–427

24. Stengel D, Bauwens K, Sehouli J, et al. (2001) Discriminatorypower of 3.5 MHz convex and 7.5 MHz linear ultrasound probesfor the imaging of traumatic splenic lesions: a feasibility study. JTrauma 51:37–43

25. Schiemann U (2004) Ultrasound in emergency patients: betterdetection of free intraabdominal fluids by use of tissue harmonicimaging. Eur J Med Res 30:328–332

26. Blaivas M, DeBehnke D, Sierzenski PR, et al. (2002) Tissue har-monic imaging improves organ visualization in trauma ultrasoundwhen compared to standard ultrasound mode. Acad Emerg Med9:48–53

27. Nilsson A, Loren I, Nirhov N, et al. (1999) Power Doppler ultra-sonography: alternative to computed tomography in abdominaltrauma patients. J Ultrasound Med 18:669–672

28. Catalano O, Lobianco R, Sandomenico F, et al. (2003) Splenictrauma: evaluation with contrast-specific sonography and a second-generation contrast medium: preliminary experience. J UltrasoundMed 22:467–477

29. Catalano O, Lobianco R, Mattace Raso M, et al. (2005) Blunthepatic trauma: evaluation with contrast-enhanced sonography. JUltrasound Med 24:299–310

30. Oldenburg A, Hohmann J, Skrok J, et al. (2004) Imaging of pae-diatric splenic injury with contrast-enhanced ultrasonography. Pe-diatr Radiol 34:351–354

31. Blaivas M, Lyon M, Brannam L, et al. (2005) Feasibility of FASTexamination performance with ultrasound contrast. J Emerg Med29:307–311

32. Yao DC, Jeffrey RB, Mirvis SE, et al. (2002) Using contrast-en-hanced helical CT to visualize arterial extravasation after bluntabdominal trauma. AJR 178:17–20

33. Fang JF, Chen RJ, Wong YC, et al. (2000) Classification andtreatment of pooling of contrast material computed tomographicscan of blunt hepatic trauma. J Trauma 49:1083–1088

34. Willmann JK, Roos JE, Platz A, et al. (2002) Multidetector CT:detection of active hemorrhage in patients with blunt abdominaltrauma. AJR 179:437–444

35. Goldberg BB, Merton DA, Liu J-B, et al. (1998) Evaluation ofbleeding sites with a tissue-specific sonographic contrast agent:preliminary experiences in an animal model. J Ultrasound Med17:609–616

36. Liu J-B, Merton DA, Goldberg BB, et al. (2000) Contrast-enhancedtwo- and three-dimensional sonography for evaluation of intra-abdominal hemorrhage. J Ultrasound Med 21:161–169

37. Poletti PA, Platon A, Becker CD, et al. (2004) Blunt abdominaltrauma: does the use of a second-generation sonographic contrastagent help to detect solid organ injuries? AJR 183:1293–1301

38. Catalano O, Cusati B, Nunziata A, et al. (2006) Active abdominalbleeding: contrast-enhanced sonography. Abdom Imaging 31:9–16

39. Albrecht T, Blomley M, Bolondi L, et al. (2004) Guidelines for theuse of contrast agents in ultrasound—January 2004. UltraschallMed 25:249–256

40. Goan YG, Huang MS, Lin JM (1998) Nonoperative managementfor extensive hepatic and splenic injuries with significant hemo-peritoneum in adults. J Trauma 45:360–364

41. Pachter HL, Knudson MM, Esrig B, et al. (1996) Status of non-operative management of blunt hepatic injuries in 1995: a multi-center experience with 404 patients. J Trauma 40:31–38

42. Parks RW, Chrysos R, Diamond T (1999) Management of livertrauma. Br J Surg 86:1121–1135

43. Navarro O, Babyn PS, Pearl RH (2000) The value of routine fol-low-up imaging in pediatric blunt liver trauma. Pediatr Radiol30:546–550

44. Cuff RF, Cogbill TH, Lambert PJ (2000) Nonoperative manage-ment of blunt liver trauma: the value of follow-up abdominalcomputed tomography scans. Am Surg 66:332–336

45. Mizzi A, Shabani A, Watt A (2002) The role of follow-up imagingin paediatric blunt abdominal trauma. Clin Radiol 57:908–912

46. Miele V, Buffa V, Stassolla A, et al. (2004) Contrast enhancedultrasound with second generation contrast agent in traumatic liverlesions. Radiol Med 107:82–91

47. Kim JH, Eun HW, Lee HK, et al. (2003) Renal perfusion abnor-mality. Coded harmonic angio US with contrast agent. Acta Radiol44:166–171


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