Hepatic Arery Vasospasm | Medical Ultrasound

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Hepatic Artery Vasospasm following Transplantation (Liver)
  Doppler Ultrasonographic Findingson Hepatic Arterial VasospasmEarly After Liver Transplantation Wei Chen, MD, RDMS, RVT, Marcelo E. Facciuto, MD, Juan P. Rocca, MD,Michael R. Marvin, MD, Patricia A. Sheiner, MD, Susan Rachlin, MD,Manuel I. Rodriguez, MD Objective. Hepatic arterial vasospasm has not been well recognized clinically as a post–liver transplantvascular complication because of the lack of sufficient data and diagnostic standards. The goal of thisstudy was to provide new evidence and a diagnostic model for the clinical appreciation of hepatic arte-rial vasospasm and evaluate the role of ultrasonography in the diagnostic process. Methods. Ninepost–orthotopic liver transplant cases were retrospectively reviewed. Multiple clinical measurementswere analyzed. Routine Doppler ultrasonography was performed within 24 hours, and additionalultrasonographic examinations were conducted as indicated. Each of the 9 patients was given a sin-gle 10 mg dose of nifedipine sublingually and monitored by ultrasonography when vasospasm wassuspected on the basis of the Doppler ultrasonographic results. Results. Doppler ultrasonographyshowed high-resistance hepatic arterial flow with absence of antegrade flow and even reversal of flowduring diastole both extrahepatically and intrahepatically in all cases. Ten to 45 minutes after admin-istration of the vasodilator, antegrade diastolic flow was observed along the course of the main hep-atic artery and its intrahepatic branches with the resistive indices decreasing on average from 1.0 to0.76. In addition, the peak systolic velocities increased from 57 cm/s before nifedipine administrationto 77 cm/s after administration. Conclusions. High-resistance hepatic arterial flow (resistive index = 1)early after liver transplantation is indicative of hepatic arterial vasospasm if it responds to vasodilators.Doppler ultrasonography is a useful tool for the diagnosis of this vascular complication. Key words: Doppler ultrasonography; hepatic artery vasospasm; high-resistance arterial flow; liver transplantation;vasodilator. Received June 20, 2005, from the Departments of Radiology and Surgery, Westchester Medical Center, Valhalla, New York USA. Revision request-ed July 22, 2005. Revised manuscript accepted for  publication December 30, 2005.We thank S. Destefano, C. Irizarry, A. Remedies,M. Scalley, and R. Singh for their contributions in performing Doppler ultrasonography. Address correspondence to Wei Chen, MD,RDMS, RVT, Department of Radiology, Westchester Medical Center, Valhalla, NY 10595 USA.E-mail: carotid01@aol.com Abbreviations DUS, Doppler ultrasonography; HAT, hepatic arterythrombosis; LFT, liver function test; MHA, main hepaticartery; OLT, orthotopic liver transplantation; PSV, peaksystolic velocity; RI, resistive index lthough hepatic arterial vasospasm has beenconsidered a potential vascular complicationafter liver transplantation experimentally, itsconcept has not been established clinically. 1 Itsincidence, mechanism, relevance, diagnosis, and prog-nosis remain to be investigated. Here we present clinicalevidence revealed by Doppler ultrasonography (DUS) in9 patients early after orthotopic liver transplantation(OLT). To our knowledge, such evidence has not beenreported previously in the English literature. These find-ings were analyzed; the value of DUS was evaluated, andthe related literature was reviewed. © 2006 by the American Institute of Ultrasound in Medicine ã J Ultrasound Med 2006; 25:631–638 ã 0278-4297/06/$3.50    A  Case Series  Materials and Methods Doppler ultrasonographic examinations andclinical data on 14 patients after OLT were retro-spectively reviewed. The 9 patients, ranging inage from 38 to 73 years, 7 male and 2 female,underwent OLT for end-stage liver disease. Thedonated livers were preserved in University of  Wisconsin solution. A standard procedure wasperformed on all patients. The donor age, indica-tion for transplantation, cold and warm ischemictimes, and liver function test (LFT) results onpostoperative days 1, 3, and 7 were recorded.Routine DUS was performed on all patients within 24 hours after transplantation at the bed-side. An HDI 3000 ultrasonography system with a5-3 MHz curved transducer (Philips MedicalSystems, Andover, MA) or a Sonoline Antaresultrasonography system with a 4V1 MHz vectortransducer (Siemens Medical Solutions, Mountain View, CA) was used. Either the transplant programor abdominal program was used. Hepatic arterialflow was examined along the course of the mainhepatic artery (MHA), the portion of the hepaticartery at the porta hepatis from the anastomosisto its bifurcation, and its major intraparenchymalbranches. Doppler waveforms were evaluated by means of the peak systolic velocity (PSV) andresistive index (RI = PSV – end-diastolic veloci-ty/PSV). 2 The absence or reversal of diastolic flow (RI = 1) within the MHA coupled with the same wave-form in the intrahepatic branches or withabsence of any intrahepatic Doppler signals war-ranted administration of a vasodilator. Among the 9 patients, 4 had nifedipine admission at thesame time as the initial ultrasonography was per-formed, and 5 patients received the vasodilatorafter additional DUS on postoperative days 2 to9. After the patient’s vital signs, including pulse,blood pressure, and P O 2 , were determined to bestable, the patient was given a single 10 mg doseof nifedipine sublingually with continued moni-toring of the vital signs. Three patients weredetermined to be unstable at the initial examina-tion; therefore, the process was postponed untilthe following day. Real-time DUS was carried outto monitor the hepatic arterial flow beginning at5 minutes after the submission of nifedipine. Thechanges of the Doppler waveforms, velocities,and RIs of the MHA and its intrahepatic branch-es were recorded and evaluated. The diagnosis of hepatic arterial vasospasm was made when apatient had a positive response to diagnosticvasodilation.Seven of the 9 patients had follow-up DUS atvarious intervals from 1 week to 2 years. Results Clinical Data Four patients were younger than 45 years, and 5 were older than 55 years. Eight (89%) of 9 donors were 55 years or older. The average cold ischemictime was 447 minutes, and the average warmischemic time was 43 minutes. The indicationsfor OLT were hepatic viral infection (5 cases and1 coexisting with hepatocellular carcinoma),cryptogenic cirrhosis (2), primary sclerosing cholangitis (1), and methotrexate toxicity (1)(Table 1). Liver function test results were consid-erably elevated compared with the standards in 632 J Ultrasound Med 2006; 25:631–638 Hepatic Arterial Vasospasm Early After Liver Transplantation Table 1. Clinical Information of 9 OLT Cases RecipientCold Ischemic Warm IschemicPatientSexAge, yDonor Age, yIndication for OLTTime, minTime, min 1M2866Cryptogenic600352M3765HCV452433M3858HCV/HCC502484F4238Cryptogenic360375M5655HCV420496M5980HBV447437M6176Methotrexate toxicity330388M6971HCV460409F7385PBC44243Median566644743Range28–7338–85330–60035–49F indicates female; HBV, hepatitis B virus; HCC, hepatocellular carcinoma; HCV, hepatitis C virus; M, male; and PBC, primary biliary cirrhosis.  our facility on postoperative day 1. There was atendency of a gradual decline on days 3 and 7(Table 2). Postoperative recovery was uneventfulin all cases. Doppler Ultrasonography  The ultrasonographic images showed highly resistant arterial flow characterized by a rapidupstroke, sharp systolic peak, and absence of antegrade flow during diastole, including rever-sal of flow leading to an RI of 1.0 in the MHA (Figure 1) in all cases and in the intrahepaticbranches (Figure 2) in 6 of the cases; intrahepat-ic flow was unobtainable in the other 3 cases. Theaverage PSVs were 54 cm/s in the MHA and 47cm/s in its branches. In 7 cases, this typicalDoppler waveform was seen immediately aftertransplantation (<24 hours), and in 2 cases, it was seen at a delayed time (5–9 days postopera-tively) after previous normal DUS findings.On administration of the vasodilator, theDoppler waveforms changed from a high-resis-tance flow pattern to a lower-resistance flow pattern extrahepatically and intrahepatically inall 9 patients (Figures 3 and 4). The average RIdecreased from 1.0 to 0.80 ( P  < .001) in the MHA and 0.75 ( P  < .001) in the intrahepatic branchesafter vasodilator administration. The velocitiesincreased from an average of 54 cm/s beforevasodilation to 84 cm/s after vasodilation ( P  <.007) in the MHA and from 47 to 60 cm/s,respectively, in the intrahepatic branches (Table3). The effective time was recorded in 5 casesand varied from 10 to 45 minutes.In 2 patients (patients 6 and 7) who had trans-plants from 80- and 85-year-old donors, theabsence of antegrade diastolic arterial flow wasshown again on follow-up DUS on postoperativedays 4 and 7, respectively. After nifedipine read-ministration, both patients again had a low-resistance waveform. Diastolic hepatic arterialflow was maintained in the other 7 patients onthe latest follow-up DUS, which ranged from 1 week to 2 years after transplantation (Table 3). Discussion Early detection and treatment of hepatic arterialcomplications is considered one of the key fac-tors affecting graft survival in the immediatepost-transplantation period. Doppler ultra-sonography is the primary imaging modality fordetection of vascular complications because it isconvenient, noninvasive, and reliable. Becausethe Doppler waveform reflects the hemodynam-ics of hepatic circulation, the changes of theDoppler waveform are associated with hepaticvascular complications, such as hepatic artery stenosis and thrombosis. 3,4  A highly resistive Doppler waveform of hepaticarterial flow is frequently found on DUS early after liver transplantation. It includes 2 cate-gories. One, seen more commonly, is decreasedbut reserved continuous diastolic arterial flow  with an abnormal RI between greater than 0.8and less than 1.0. The other, seen in a substantialpercentage but less frequently, is an absence of diastolic arterial flow (RI = 1.0) with reversal of flow. For more than a decade, studies have beendone in searching for the causes and clinical rel-evance of those DUS findings. Because the RI hasbeen used for predicting the presence of acuterejection in renal allograft recipients, someinvestigators tried to link the waveform in thefirst category to hepatic graft rejection. However,none of those studies showed that decreaseddiastolic flow could predict acute rejection inliver transplants. 5,6 The one in the second cate-gory is the most controversial finding in DUS of after OLT because it has been linked to hepaticartery thrombosis (HAT), a devastating eventrelated to a high rate of graft loss. Some authorsobserved that absent or reversed diastolic arteri-al flow appeared just before hepatic arterial flow  J Ultrasound Med 2006; 25:631–638 633Chen et al Table 2. Postoperative LFT Values Day 1Day 3Day 7 ValueASTALTTBINRASTALTTBINRASTALTTBINR Median6355189.51.902153374.01.32611153.51.15Range137–129–2.7–1.27–102–102–1.7–0.90–25–58–1.1–0.80–3611130217.910.20148084417.01.6661917717.81.71Standard LFT values in our facility: aspartate aminotransferase (AST), 4–35 U/L; alanine aminotransferase (ALT), 2–40 U/L; total bilirubin (TB),0.2–1.3 mg/dL; and international normal ratio of an individual thrombin time to a reference (INR), 1.  vanished in patients with HAT. Therefore, they suggested using this absent diastolic Doppler waveform to predict or support the diagnosis of post-transplant HAT. 7–9 However, others foundthat it was poorly associated with HAT becausethe incidence of HAT was low among patients who had this highly resistant arterial flow. 10,11 Lacking a proper model or method for investiga-tors to prove the causes, so far no one has had aclear answer to the question of what this ultra-sonographic finding means, although one reportmentioned that this phenomenon might berelated to arterial vasospasm. 11 Under physiologic conditions, the hepatic arte-rial flow shows low-resistance flow with ante-grade flow throughout diastole on DUS becauseof the broad arterio-portal and arterio-sinus con-nection in the hepatic microvascular system. 12 The RIs normally range from 0.6 to 0.7. 13  Arterial vasospasm is a state of arterial vesselconstriction. The affected segmental or entirevessel becomes rigid, and its lumen narrows oreven becomes occluded. 14  According toPoiseuille’s equation, R = 8 l  η / π r  4 , the resistance( R ) depends on the viscous properties of theblood ( η ) and on the dimensions of the vessels. Any decrease in the diameter of a vessel will sub-stantially increase its resistance because theresistance is inversely related to the fourth powerof the radius ( r  ). 15  Whenever the hepatic artery iscontracted, its diameter will correspondingly reduce, and, as a result, the resistance of the hep-atic arterial flow will increase. The same principleof vascular hemodynamics can be also applied toHAT. If arterial flow is obstructed distally by thrombosis, high-resistant arterial flow will beobtained proximally to the obstructed site. 9 Thismeans that during certain circumstances, HATmay share a common DUS appearance, absenceof antegrade diastolic flow with reversal of flow, with hepatic arterial vasospasm. Garcia-Criadoet al 16 reported that 4 of 10 asymptomaticpatients with HAT had this kind of flow pattern atthe early post-OLT stage. All the patients in ourstudy shown highly resistant flow with an RI of 1.0 in the MHA. The absence of diastolic flow was 634 J Ultrasound Med 2006; 25:631–638 Hepatic Arterial Vasospasm Early After Liver Transplantation Figure 1. Image from patient 6. Typical Doppler waveformswere obtained from the MHA before vasodilation early after livertransplantation. The characteristics of the Doppler waveformwere a rapid upstroke, a sharp systolic peak, and absence ofantegrade flow with a reversal component during diastole. Figure 2. Image from patient 5. The same arterial Dopplerwaveforms seen in the MHA were shown intrahepatically beforevasodilation in 6 cases. Figure 3. Image from patient 6. On administration of thevasodilator, antegrade diastolic flow was observed along thecourse of the MHA.
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