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Original Research |
1 Department of Radiology, Asan Medical Center, University of Ulsan College of
Medicine, 388-1, Pungnap-dong, Songpa-ku, Seoul 138-736, Korea.
2 Department of Radiology, Hallym University Sacred Heart Hospital, Anyang,
Korea.
3 Department of Radiology and Institute of Radiation Medicine, Seoul National
University College of Medicine, Seoul, Korea.
4 Department of Radiology, Severance Hospital, Yonsei University College of
Medicine, Seoul, Korea.
5 Department of Medical Imaging, Toronto General Hospital, Toronto, ON,
Canada.
Received April 6, 2006;
accepted after revision March 26, 2007.
Address correspondence to K. W. Kim
(kimkw{at}amc.seoul.kr).
Abstract
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SUBJECTS AND METHODS. The study group included 352 patients who underwent Doppler sonography after 361 percutaneous liver biopsies. Color-flow images were obtained immediately and 5 minutes after the biopsies. Images were evaluated for the patent track sign, defined as linear color flow along the needle path. Patients were followed-up with clinical and laboratory findings to search for postbiopsy bleeding. Those suspected of having postbiopsy bleeding underwent CT. Sonographic results were compared with clinical and CT findings.
RESULTS. Clinically significant postbiopsy bleeding occurred in five patients (1%). On Doppler sonography immediately after the biopsies, the patent track sign was seen in 43 patients (12%). Patients with this sign more frequently bled than those without it (p = 0.0008). Sensitivity, specificity, positive predictive values, and negative predictive values in detection of postbiopsy bleeding were 80%, 89%, 9%, and 100%, respectively. Among these patients, this sign was persistently seen in four and disappeared in the remaining 39 at 5 minutes after the biopsies. Patients with a persistent patent track sign more frequently bled than those without it (p < 0.0001). Sensitivity, specificity, positive predictive value, and negative predictive value were 60%, 100%, 75%, and 99%, respectively.
CONCLUSION. A patent track sign, frequently seen on Doppler sonography immediately after percutaneous liver biopsy, provides excellent screening for postbiopsy bleeding. This sign strongly predicts postbiopsy bleeding when persistently seen for 5 minutes.
Keywords: Doppler sonography • liver • "patent track" sign • percutaneous liver biopsy
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Early detection of postbiopsy bleeding, if such bleeding occurs, is important for proper management in these patients to prevent a catastrophic result. In general, the detection of postbiopsy bleeding has been made on the basis of suggestive clinical symptoms and signs such as shock or hypotension and a drop in serum hemoglobin concentration [3]. Sonography may be helpful in disclosing profuse hepatic parenchymal bleeding and bleeding into the peritoneal cavity [9, 10], and it is generally agreed that CT is better than sonography for that purpose [11].
Doppler sonography has been shown to be a sensitive method for detection of postbiopsy complications such as arterial pseudoaneurysm and arteriovenous fistula after percutaneous vascular and nonvascular puncture [12, 13]. However, these examinations usually have been performed only in selected patients with clinical suspicion of serious postbiopsy complications. Although it has been observed that a linear colorflow signal may be seen along the needle track immediately after needle withdrawal [14-16], the prevalence of this finding and its predictive role in detection of postbiopsy bleeding has not been determined. We defined this finding as a "patent track" sign and, thus, the purpose of this study was to determine the prevalence of the patent track sign on Doppler sonography after percutaneous transcapsular liver biopsy and to assess the value of this sign in detection of clinically significant postbiopsy bleeding.
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In all patients, laboratory values, including peripheral coagulation studies such as platelet count and prothrombin time and baseline serum hemoglobin concentration level, were obtained within a week before the biopsy procedures. The normal range of platelet count was 150,000-300,000/mm3 (Thrombocounter, Coulter Electronic Co.), and thrombocytopenia was defined as a platelet count of less than 150,000/mm3. One hundred five patients with 108 biopsies (29%) had thrombocytopenia. Prothrombin time results were expressed as percentage activity; the lower range of normal was 70% (Thromborel S [human thromboplastin], Behring Institute), and it was defined as being elongated when it was less than 70%. Forty-nine patients with 52 biopsies (14%) had elongation of prothrombin time. Thirty-five patients with 36 biopsies (10%) had both thrombocytopenia and elongation of prothrombin time.
Percutaneous Liver Biopsy Methods
The patients fasted from the midnight before and until 8 hours after the
biopsies, and they did not receive any premedication. In all patients,
informed written consent to perform the liver biopsy was obtained at least 24
hours before the biopsy procedure. The patients with coagulopathy underwent
prophylactic transfusion of platelet concentrates or fresh frozen plasma
before the biopsies, and coagulation studies were repeatedly done before the
biopsies.
The biopsies were performed under real-time sonographic guidance with a freehand technique by two experienced abdominal radiologists (> 100 biopsies each), using commercially available equipment such as HDI 3000 and 5000 units (Philips Medical Systems) (n = 133), a Logiq 700 unit (GE Healthcare) (n = 36), and a Sequoia 512 unit (Acuson) (n = 192). A 2-4-MHz or a 1-4-MHz curved array transducer was used in most cases, and a 7-15-MHz linear array transducer was occasionally used for biopsies of small, superficially located (< 5 cm) focal hepatic lesions. The entire biopsy procedure was performed under aseptic conditions.
The optimal sites for the puncture and needle path were selected by sonography to avoid large interposed blood vessels in the needle track and highly vascular areas within the focal lesion. A local anesthetic, Xylocaine (lidocaine hydrochloride, Astra), was injected from the puncture site along the entire needle path into the liver with a 22-gauge spinal needle. Thereafter, a 10- or 15-cm 18-gauge Tru-cut needle (Automated Cutting Needle, Medical Device Technologies) was inserted along the anesthetized track to the edge of the target point under sonographic guidance while the patient resumed shallow breathing.
After proper placement of the needle, automated biopsies were performed with the patient in suspended respiration. In general, two passes were obtained to ensure a representative histopathologic sample, and additional passes were occasionally obtained in biopsies of focal hepatic lesions if prior passes were deemed insufficient until the tissue appeared diagnostic for focal abnormality. For biopsies of focal hepatic lesions, normal liver tissues were traversed before the masses were entered to avoid possible peritoneal tumor spillage or tumoral bleeding.
Doppler Sonographic Examination
The routine prospective Doppler sonographic examinations were performed
after the biopsy procedures, along with forceful compression at the puncture
site. The same radiologists who performed the biopsies performed the
examinations with the same equipment and transducers used for biopsy guidance,
and they were not blinded to the information about coagulation indexes.
Immediately after withdrawal of the biopsy needle, the needle track was
identified by gray-scale sonography, and color Doppler sonograms were obtained
and analyzed to determine the presence or absence of an immediate patent track
sign, which was defined as a linear color-flow signal toward the liver capsule
along the needle track (Figs.
1A and
1B). The color Doppler
sonography parameters were individually adjusted for each patient to maximal
gain without background noise, highest pulse-repetition frequency without
aliasing artifacts, and medium wall filter. The color-encoded area was
restricted as much as possible to cover the entire needle path. When an
immediate patent track sign was seen on color Doppler sonography, we tried to
obtain a spectral Doppler waveform in the track with the patient in
breath-hold.
In all patients, color Doppler sonograms were repeatedly obtained 5 minutes after the biopsies. The images were analyzed to determine the presence or absence of a persistent patent track sign. Thereafter, examination time per patient varied according to the presence or absence of the persistent patent track sign. When there was absence of a persistent patent track sign, we obtained additional gray-scale sonograms of the hepatic parenchyma and peritoneal recesses (subphrenic, hepatorenal, right paracolic, and paravesical spaces) in search of the possible presence of intrahepatic hematoma or peritoneal blood effusion and finished the examination. When a persistent patent track sign was present, the examination continued up to 25 minutes with forceful manual compression toward the track to see whether this sign resolved or not. Additional gray-scale sonograms of hepatic parenchyma and peritoneal recesses were also obtained before the end of the examination.
Reference Diagnoses
Eighteen potential donors for liver transplantation without coagulopathy
underwent biopsies for grading of fatty infiltration on an outpatient basis.
After completion of Doppler sonography and the biopsy procedure, the patients
were detained outside the operating room and were allowed to leave the
hospital 4 hours after the procedures if they had no unusual clinical symptoms
or signs suggestive of postbiopsy complications. The remaining 334 patients
underwent biopsies during their hospitalization periods, and none of them were
discharged earlier than 24 hours after the biopsy. After the biopsies and
Doppler sonography, the patients were asked to lie on the side of the puncture
for 6-8 hours and to remain supine for that evening and night. Clinical
symptoms, blood pressure, and heart rate were monitored. In 44 patients,
follow-up serum hemoglobin level was obtained within 8 hours (range, 1-8
hours; mean, 3 hours) after the biopsies. In the remaining 290 patients, those
values were obtained within a week (range, 1-7 days; mean, 2 days) after the
biopsies. The patients with unequivocal clinical signs of hemorrhage, such as
shock or an otherwise unexplained drop in serum hemoglobin concentration of
greater than 1 g/dL, were clinically suspected of having a biopsy-related
bleeding event and underwent CT examinations. CT scans were obtained with an
MDCT scanner (LightSpeed QX/i, GE Healthcare) before and after bolus injection
of 120 mL of iopromide (Ultravist 370, Schering). CT scans were evaluated by
two experienced abdominal radiologists in search of evidence of postbiopsy
bleeding such as intrahepatic or intraperitoneal hematoma and active
extravasation of IV contrast agent.
Statistical Analyses
Statistical analyses were performed with commercially available standard
statistical software (SPSS for Windows, version 10.0). To assess whether there
were significant relationships between peripheral coagulation indexes or
patent track sign on Doppler sonography and the subsequent occurrence of
clinically significant postbiopsy bleeding, analyses were performed with
Fisher's exact test using the reference diagnoses as the standard reference.
Sensitivity, specificity, positive predictive value, and negative predictive
value of the patent track sign for detection of clinically significant
postbiopsy bleeding were assessed, and these values were compared with those
of peripheral coagulation indexes. The mean differences in peripheral
coagulation indexes between the two groups with and without a patent track
sign on Doppler sonography were compared using the Student's t test.
For patients in whom information on spectral Doppler sonography was available,
the relationship between whether the spectral Doppler sonography in the track
showed a pulsatile arterial waveform or a monophasic venous waveform and the
subsequent occurrence of postbiopsy bleeding was evaluated by Fisher's exact
test as well. Significance was indicated if a two-tailed p value was
less than 0.05.
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Among the five patients with clinically significant postbiopsy bleeding, one had both thrombocytopenia and elongation of prothrombin time, three had thrombocytopenia and normal prothrombin time, and the other patient had a normal platelet count and elongation of prothrombin time. Although there was no significant relationship between elongation of prothrombin time alone and the subsequent occurrence of postbiopsy bleeding events (p = 0.1528), the patients with thrombocytopenia alone and those with either thrombocytopenia or elongation of prothrombin time more frequently bled than the others (p = 0.0136 and 0.0045, respectively). The sensitivity, specificity, positive predictive value, and negative predictive value of each peripheral coagulation index and its combination in detection of clinically significant postbiopsy bleeding are shown in Table 2.
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On color Doppler sonograms obtained immediately after biopsy needle withdrawal, a patent track sign was seen in 43 cases (12%). Among these patients, clinically significant postbiopsy bleeding occurred in four, whereas the event occurred in only one of 318 patients without this sign. There was a significant relationship between the presence or absence of the patent track sign and the subsequent occurrence of postbiopsy bleeding events (p = 0.0008). The diagnostic values of the patent track sign in the prediction of postbiopsy bleeding are shown in Table 2.
Although the mean platelet count for patients with the patent track sign on Doppler sonograms immediately after the biopsy needle withdrawal was 172,600 ± 124,200/mm3 (range, 37,000-733,000/mm3), that value for the patients without the patent track sign was 216,900 ± 99,400/mm3 (range, 29,000-621,000/mm3). The difference was statistically significant (p = 0.0085). Although the mean prothrombin time for patients with the patent track sign on Doppler sonograms immediately after the biopsy needle withdrawal was 78.0% ± 16.1% (range, 36-108%), that value for the patients without the patent track sign was 86.7% ± 14.3% (range, 39.6-130%). The difference was statistically significant as well (p = 0.0003). Of 27 patients in whom information on spectral Doppler sonography was available, 12 had a pulsatile arterial waveform and the other 15 had a monophasic venous waveform in the track. There was no significant relationship between whether spectral Doppler sonography in the track showed a pulsatile arterial waveform or a monophasic venous waveform and the subsequent occurrence of postbiopsy bleeding (p = 0.57).
Among the 43 patients with a patent track sign on the images immediately after the biopsy needle withdrawal, this sign was persistent in four and transient in the remaining 39 on color Doppler sonograms obtained 5 minutes after the biopsy. None of the patients without the patent track sign on the former examination had this sign on the latter. The postbiopsy bleeding events were more significantly related to the presence of a persistent patent track sign (p < 0.0001) than the presence of this sign immediately after the needle withdrawal (p = 0.0008). All four patients with a persistent patent track sign had information on spectral Doppler waveform, which was arterial in three and venous in the other one. However, there was no significant relationship between whether spectral Doppler sonography in the track showed a pulsatile arterial waveform or a monophasic venous waveform and the subsequent occurrence of postbiopsy bleeding (p = 1.0000).
In our series, a persistent patent track sign did not resolve with forceful manual compression toward the track until up to 25 minutes. Gray-scale sonograms also showed intrahepatic hematoma (n = 1), abdominal wall hematoma (n = 1), and perihepatic free fluid (n = 2) in patients with a persistent patent track sign. Although perihepatic free fluid was also seen in another two patients without a patent track sign, serious bleeding complications did not occur in these patients.
Among the five patients with postbiopsy bleeding events, two patients with a persistent patent track sign with pulsatile arterial waveform in the track improved after prompt surgical exploration and hemostasis. Another one with a persistent patent track sign with a pulsatile arterial waveform underwent percutaneous hepatic arterial embolization with gelatin sponge particles of approximately 1 mm3 (Spongostan, Johnson & Johnson Medical), but clinical signs of postbiopsy bleeding persisted and a drop in serum hemoglobin concentration continued. Therefore, the patient underwent laparoscopic hemostasis 5 days after the biopsy and improved thereafter. Another patient with a persistent patent track sign with a monophasic venous waveform improved with conservative medical management consisting of close clinical monitoring and continuous transfusion. However, the other patient who showed a transient patent track sign only immediately after needle withdrawal and who presented with delayed onset of postbiopsy bleeding rapidly deteriorated despite massive transfusion and percutaneous hepatic arterial embolization with gelatin sponge particles and eventually died.
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Sonography is the preferred imaging technique for guiding a needle into a liver target lesion during percutaneous liver biopsy because of its well-known characteristics, such as real-time examination, ability to change the scanning plane, and low cost. In addition to improved diagnostic accuracy [1, 2], by using color Doppler sonography, one can avoid puncture of critical blood vessels interposed in the path to a lesion during the needle biopsy, which is important to diminish the risk of postbiopsy bleeding [14, 18].
On the other hand, the role of sonography in the detection of postbiopsy bleeding has been subject to debate. Several investigators have shown that in the presence of clinical signs of postbiopsy complications sonography should be repeated and may be helpful in disclosing profuse parenchymal hemorrhage and bleeding into the peritoneal cavity from 2 to 24 hours after the biopsies [9, 10].
Although it has been shown that, after needle withdrawal, color Doppler sonography may reveal a linear track of color flow toward the liver capsule along the needle track signal, allowing prompt detection of postbiopsy bleeding [14-16], it also has been shown that this finding may resolve spontaneously without subsequent occurrence of postbiopsy bleeding [15]. Therefore, this examination is not routinely performed in many institutions. In this study, we defined this finding as a patent track sign and attempted to determine the prevalence of this sign after percutaneous liver biopsy and to assess its diagnostic value in the detection of postbiopsy bleeding.
In our results, a patent track sign was not infrequently seen (12%) on Doppler sonography immediately after the biopsy needle withdrawal and was more frequently seen in patients with thrombocytopenia (p = 0.0085) or elongation of prothrombin time (p = 0.0003). The patients with this sign more frequently bled than those without this sign (p = 0.0008), and it produced 80% sensitivity and 89% specificity in the detection of clinically significant postbiopsy bleeding. Although the positive predictive value of this sign was very low (9%), it was slightly higher than those of peripheral coagulation indexes, and the negative predictive value reached 100%.
We assume that visualization of this sign after percutaneous liver biopsy may imply the presence of risk factors of postbiopsy bleeding, such as tumoral hypervascularity and injury of blood vessels interposed in the needle path during the biopsy procedure, in addition to the intrinsic bleeding diathesis of the patient. Therefore, we believe that Doppler sonography immediately after the biopsy needle withdrawal may provide more effective screening for the selection of patients who are at risk of postbiopsy bleeding than peripheral coagulation indexes. This examination may be especially helpful in the biopsy of patients with coagulopathy because the absence of this sign may indicate that the biopsy was performed safely, whereas the presence of this sign still warns of postbiopsy bleeding. Also, although this sign usually resolved spontaneously during the 5 minutes of Doppler sonography examination with compression of the puncture site in patients with uncomplicated cases, it was highly predictive (75%) of a subsequent occurrence of postbiopsy bleeding when it was persistently seen for 5 minutes after the biopsy.
In our series, the information on spectral Doppler waveform was available in 27 of 43 patients with the patent track sign immediately after biopsy needle withdrawal. It was not available in the other 16 patients because this sign rapidly resolved during the examination before the Doppler sonography spectrum was obtained. However, there was no significant relationship between whether the spectral Doppler sonography in the track showed a pulsatile arterial waveform or a monophasic venous waveform and the subsequent occurrence of postbiopsy bleeding (p = 0.57).
There are several points that deserve special mention in our study. First, the incidence of clinically significant postbiopsy bleeding (1%) and mortality (0.3%) were relatively high compared with prior reports. In several large, mostly retrospective series, the reported incidence of serious bleeding complications ranged from 0.06% to 1.7% of the cases and the mortality rate was between 0.009% and 0.48% [3-5]. However, based on previous reports, the exact risk of postbiopsy bleeding cannot precisely be determined because accepted limits of coagulation status varied considerably, and patients with severe clotting disturbances are not generally biopsied. Therefore, the relatively high incidence of serious bleeding complications and mortality in our series may be attributed to the high proportion of coagulopathy in patients included in this study. Moreover, when a persistent patent track sign was present, we did forceful manual compression toward the track to see whether this sign resolved or not, although there has been no bibliographic evidence that this maneuver has any hemostatic role after liver biopsy. Because applying direct pressure is not possible in cases of liver biopsy performed by means of an intercostal approach, this maneuver may have delayed timely application of a sandbag with patients lying on the affected side, which might have provided some tamponade effect [16].
Second, the overall incidence of postbiopsy bleeding, including subclinical minor hemorrhage, could not be assessed in our study because we focused on the detection of clinically significant postbiopsy bleeding. Therefore, only patients with unequivocal clinical signs of hemorrhage such as shock or an otherwise unexplained drop in serum hemoglobin concentration of greater than 1g/dL underwent CT examinations.
Third, the results of our study can only be extrapolated to biopsies with 18-gauge needles of the Tru-cut type because we did not use any other types of needles or different diameters. Fourth, because the same radiologists performed the biopsy and Doppler sonography, they were unblinded to the information about platelet count and prothrombin time at the time of examination, which may have interfered with postbiopsy Doppler sonography analysis. Fifth, we have not considered other bleeding risks such as ascites or portal hypertension. However, the purpose of our study was not to determine the risk factors of postbiopsy bleeding, which may sometimes contraindicate the percutaneous biopsy, but to assess the value of Doppler sonography, which may be helpful in assessing the safety of performed biopsies frequently needed in patients with risk factors.
In conclusion, a patent track sign on Doppler sonography immediately after percutaneous liver biopsy is frequently seen in patients with coagulopathy and provides excellent screening for early detection of postbiopsy bleeding. Also, the presence of this sign strongly predicts the subsequent occurrence of clinically significant postbiopsy bleeding when it is persistently seen for 5 minutes after the biopsy. Therefore, for a timely and appropriate intervention on this condition, Doppler sonography should be routinely performed after percutaneous liver biopsy.
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