DOI:10.2214/AJR.04.1395
AJR 2005; 185:878-884
© American Roentgen Ray Society
Postbiopsy Splenic Bleeding in a Dog Model: Comparison of Cauterization, Embolization, and Plugging of the Needle Tract
Seung Hong Choi1,
Jeong Min Lee1,
Kyoung Ho Lee2,
Se Hyung Kim1,
Jae Young Lee1,
Joon Koo Han1 and
Byung Ihn Choi1
1 Department of Radiology and Institute of Radiation Medicine, Seoul National
University College of Medicine, Clinical Research Institute, Seoul National
University Hospital, 28 Yongon-dong, Chongno-gu, Seoul 110-744,
2 Department of Radiology, Seoul National University Bundang Hospital, Seoul,
Korea.
Received September 2, 2004;
accepted after revision November 10, 2004.
Address correspondence to J. M. Lee
(leejm{at}radcom.snu.ac.kr).
Supported by grant number 04-2002-031-0 from the Seoul National University
Hospital research fund.
Abstract
OBJECTIVE. The purpose of our study was to compare radiofrequency
cauterization, embolization using an absorbable gelatin sponge, and a
Histoacryl-Lipiodol mixture plugging as postbiopsy bleeding reduction methods
after splenic core needle biopsy in a dog model.
MATERIALS AND METHODS. Eleven mongrel dogs were randomly separated
into nonheparinized (n = 5) and heparinized (n = 6) groups.
Eight splenic biopsies per animal were performed using an 18-gauge automated
core biopsy needle: two as controls, two ablated by radiofrequency, two
embolized using an absorbable gelatin sponge, and two plugged using a
Histoacryl-Lipiodol mixture. Procedure times and postbiopsy bleeding amounts
were assessed. Statistically significant differences were determined by
repeated measures analysis of variance; the Tukey-Kramer test for multiple
comparisons was used for post hoc comparisons. Three-day follow-up CT scans
were obtained to check for procedure-related complications or delayed
bleeding.
RESULTS. The postbiopsy bleeding reduction groups showed
significantly less blood loss than the control group for both the
nonheparinized (p < 0.0001) and heparinized groups (p
< 0.0001). In the heparinized group, both radiofrequency cauterization
(p < 0.01) and gelatin sponge embolization (p < 0.05)
significantly reduced bleeding compared with Histoacryl-Lipiodol mixture
plugging. Gelatin sponge embolization was the longest procedure (p
< 0.001). On follow-up CT, no delayed bleeding was observed. However,
multiple Histoacryl-Lipiodol emboli were observed in the splenic and portal
veins in all the dogs we treated.
CONCLUSION. Radiofrequency cauterization was found to be the most
useful postbiopsy bleeding reduction method in terms of the amount of bleeding
and the procedure time.
Introduction
Percutaneous biopsy is an important diagnostic procedure in modern
medicine. One of the more common indications for abdominal biopsy is the need
to obtain a tissue diagnosis in patients with focal or diffuse disease
[1]. However, splenomegaly and
focal splenic lesions may develop in immunosuppressed or immunodeficient
patients and those with a history of malignancy, risk of metastases, or
relapse. The nature of the splenic lesions is of primary diagnostic importance
and often defines the course of treatment in these patients
[2-4].
In the past, fine-needle aspiration biopsy of the spleen was performed in
patients with splenomegaly or focal splenic lesions; it has been accepted as a
simple, safe, and well-tolerated procedure. However, reported diagnostic
yields using a 22- or 23-gauge needle vary from 15% to 100%
[5-8].
Sonographically guided core biopsy of the spleen is a relatively new procedure
for sampling target lesions, and one that retains the architectural
relationships and stromal elements for histopathologic evaluation. Various
studies [2,
3,
9] have shown 97.8-100%
diagnostic yields, with 0-12.5% complication rates. However, despite the high
diagnostic yield of percutaneous splenic biopsy, it is often avoided by
radiologists because many perceive that complication risks, particularly of
hemorrhage, are high compared with biopsies of other abdominal organs
[10,
11]. In addition, the risk of
postbiopsy hemorrhagic complications is particularly great in patients with
therapeutic or pathologic coagulopathy.
Recently, several methods have been proposed to reduce postbiopsy bleeding
in the abdominal solid organs
[1,
12-17].
These methods include plugging the biopsy tract using a hemostatic agent such
as an absorbable gelatin sponge, a coil, fibrin sealants, or a
Histoacryl-Lipiodol mixture, and the application of radiofrequency energy to
occlude the biopsy tract. Each of these techniques has been described as an
effective postbiopsy bleeding reduction method
[12-17].
To our knowledge, however, no study has been undertaken to compare the
performances of these techniques with respect to bleeding reduction after a
core needle biopsy of the spleen.
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Fig. 1A —Radiofrequency cauterization of splenic biopsy tract.
Photograph of 15-gauge introducer sheath shows stainless insulation, leading
8-mm uninsulated region (straight arrow), and transducer (curved
arrow) used to connect radiofrequency generator.
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The purpose of this investigation was to compare radiofrequency
cauterization, splenic biopsy tract embolization using an absorbable gelatin
sponge (Gelfoam, Upjohn), and a Histoacryl-Lipiodol (tissue adhesive, B.
Braun-iodized oil, Guerbet) mixture plugging as bleeding reduction methods
after splenic core needle biopsy in a dog model.
Materials and Methods
Animals and Animal Preparation
The experimental protocols used in this study were approved by the
committee on animal research at our institution. Eleven mongrel dogs (12-16
months old, 16-20 kg, all female) were randomly allocated into one of two
groups: nonheparinized (n = 5) and heparinized (n = 6). In
dogs in the former group, heparin was not administered and blood sampling was
performed once before the experiment. In the heparinized group, a bolus of 300
U of heparin per kilogram of body weight was administered IV resulting in an
anticoagulated state. Blood samples were taken before and after the
administration of heparin. Seventeen samples (five from the nonheparinized
group and 12 from the heparinized group) were tested for RBC, hemoglobin
level, hematocrit level, platelet count, prothrombin time, and activated
partial thromboplastin time.
Each animal was anesthetized with an intramuscular injection of 10 mg/kg of
ketamine hydrochloride (Ketalar, Yuhan Yanghang) and 4 mg/kg of xylazine
hydrochloride (Rompun, Bayer Korea). Endotracheal intubation was performed and
anesthesia was maintained with inhaled enflurane gas (Gerolan, Choongwae
Pharma), 1.5% to effect. After application of a 10% povidone-iodine solution,
the spleen was exposed through a midline incision.
Study Design
Eighty-eight biopsies (eight biopsies per dog) were performed using an
18-gauge automated side-cutting core biopsy needle (Acecut, TSK). The
penetrating depth was 2.5 cm, and the biopsy window was 15 mm. Different core
biopsy needles were used for each animal. Each dog underwent eight biopsies
consisting of two controls (without bleeding reduction in the biopsy needle
tract), and six with postbiopsy bleeding reduction: two ablated by
radiofrequency, two embolized using an absorbable gelatin sponge, and two
plugged with a Histoacryl-Lipiodol mixture in the splenic biopsy tracts.
Biopsy was performed sequentially, one biopsy without a hemostatic procedure
followed by one biopsy each of radiofrequency cauterization, gelatin sponge
embolization, and Histoacryl-Lipiodol mixture plugging. Each procedure was
then repeated once more. Biopsy procedure times were recorded, and the biopsy
sites were photographed to allow correlation with CT findings. Blood loss from
each biopsy site was assessed visually and also by weighing dry gauze pads
used to soak up any blood from the puncture sites and then reweighing the
gauze pads plus the blood. Biopsy sites were sutured if hemostasis had not
been achieved within 1 hr.
Three-day follow-up CT scans were obtained. CT images were reviewed by an
abdominal radiologist using our PACS (Maroview, Marotech). CT images were
evaluated with regard to parenchymal changes of the splenic biopsy sites and
the presence of delayed postbiopsy bleeding at the biopsy sites. Other
abdominal organs were also evaluated.
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Fig. 2A —Histoacryl-Lipiodol (tissue adhesive, B. Braun-iodized oil,
Guerbet) mixture plugging in splenic biopsy tract. Photographs show 18-gauge
biopsy needle placed through its vascular sheath (A), splenic biopsy
procedure needle and vascular sheath complex (B), and
Histoacryl-Lipiodol mixture plugging of splenic biopsy site after biopsy
needle removal (C).
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Fig. 2B —Histoacryl-Lipiodol (tissue adhesive, B. Braun-iodized oil,
Guerbet) mixture plugging in splenic biopsy tract. Photographs show 18-gauge
biopsy needle placed through its vascular sheath (A), splenic biopsy
procedure needle and vascular sheath complex (B), and
Histoacryl-Lipiodol mixture plugging of splenic biopsy site after biopsy
needle removal (C).
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Fig. 2C —Histoacryl-Lipiodol (tissue adhesive, B. Braun-iodized oil,
Guerbet) mixture plugging in splenic biopsy tract. Photographs show 18-gauge
biopsy needle placed through its vascular sheath (A), splenic biopsy
procedure needle and vascular sheath complex (B), and
Histoacryl-Lipiodol mixture plugging of splenic biopsy site after biopsy
needle removal (C).
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Postbiopsy Bleeding Reduction Procedures
Radiofrequency cauterization of splenic biopsy tract—A
15-gauge metallic introducer sheath, which was manufactured for this
experiment by a medical company (Taewoong), was insulated electrically with
stainless steel, leaving the leading 8 mm of the needle uninsulated to allow
radiofrequency application. The trailing portion of this introducer sheath was
composed of a transducer connected to a 500-KHz monopolar radiofrequency
generator (CC-1, Radionics) that was able to produce 200-W output
(Fig. 1A).
An appropriate site was chosen, and the biopsy needle was inserted through
a 15-gauge introducer sheath. The needle and sheath complex were advanced
approximately 1 cm inside the spleen. The sheath was held firmly fixed to the
needle during advancement; the biopsy was then performed in the standard
manner (Fig. 1B). After the
biopsy specimen was obtained, the sheath was then advanced to the needle tip
and the needle was removed, leaving the sheath in place. In this treatment
trial, the introducer sheath was held stationary as radiofrequency energy with
power of 100 W was applied (Fig.
1C). Tissue impedance was continuously monitored by means of the
circuitry in the radiofrequency generator. When radiofrequency energy
instillation induced a rapid increase in the tissue impedance, suggesting
boiling and charring of the tissue adjacent to the sheath, radiofrequency
application was discontinued and the introducer sheath was withdrawn slowly by
8 mm. Radiofrequency energy was then delivered to the proximal biopsy tract
with impedance monitoring.
Histoacryl-Lipiodol mixture plugging of splenic biopsy
tract—An appropriate site was chosen, and the biopsy needle was
inserted through a 5-French vascular introducer sheath (Cordis)
(Fig. 2A). The needle and
sheath complex were advanced approximately 1 cm into the spleen, with the
sheath firmly fixed to the needle. Biopsies were then completed in the
standard manner (Fig. 2B).
After obtaining a biopsy specimen, the sheath was advanced to the needle tip
and the needle was removed, leaving the sheath in place. Histoacryl and
Lipiodol were then mixed in a 1:3 ratio, and 1 mL of this Histoacryl-Lipiodol
mixture was injected through the sheath without withdrawal so as to fill the
sheath (Fig. 2C). The mixture
remaining in the sheath was then ejected by injecting a 5% glucose solution
(0.7 mL) with controlled sheath withdrawal.
Splenic biopsy tract embolization using absorbable gelatin
sponge—After a splenic biopsy specimen was obtained using the
method just described, the hemostatic valve of the vascular sheath was removed
to allow the passage of a block of gelatin sponge in the vascular sheath
(Fig. 3). A block of absorbable
gelatin sponge was manually cut into strips approximately 2 cm in length,
tightly rolled by hand, and loaded into the vascular sheath. The dilator
supplied with the vascular sheath was used to push the loaded gelatin sponge
into the vascular sheath, where it was deposited in the splenic parenchyma as
the sheath was slowly removed. Four to six pieces of gelatin sponge were used
at each biopsy site. The sheath was withdrawn as the embolizing absorbable
gelatin sponge was placed in the tract.
CT
Anesthesia for CT was induced with an intramuscular injection of 10 mg per
kilogram of body weight of ketamine hydrochloride (Ketalar) and 4 mg/kg of
xylazine hydrochloride (Rompun 2%), and anesthesia was maintained with an IV
injection of 10 mg/kg of zolazepam (Zoletil, Virbac). The antecubital vein was
catheterized with an 18-gauge plastic cannula for contrast material injection.
CT scans were acquired during quiet self-breathing after endotracheal
intubation.
Two-phase helical CT (Somatom Plus 4, Siemens Medical Solutions) was
performed with the dogs in the supine position using the following scanning
parameters: 120 kVp; 200 mA; table feed, 5 mm; collimation, 3 mm; and
reconstruction interval, 2 mm. Initially, unenhanced CT scans were obtained.
After injecting 2.5 mL/kg of contrast material ([iopromide] Ultravist 370,
Schering) at a rate of 2 mL/sec, arterial phase scanning was initiated using a
bolus tracking method 5 sec after aortic attenuation exceeded 100 H. Portal
phase scanning was initiated 15 sec after arterial phase scanning. This CT
protocol was chosen on the basis of results obtained from preliminary
single-level dynamic scanning. Animals were sacrificed after follow-up CT
acquisition by IV administration of a lethal amount of thiopental sodium
(Pentothal, Choongwae Pharm).
Statistical Analysis of Bleeding Amount
Statistical analysis was performed using commercially available software
(Instat, version 3.05; GraphPad Software). Tests for significant differences
in procedure times for the three postbiopsy bleeding reduction maneuvers and
in blood losses in the control and postbiopsy bleeding control groups were
performed using repeated measurements analysis of variance. The Tukey-Kramer
test was used for multiple post hoc comparisons. The Student's t test
was used to assess differences in bleeding amounts in heparinized and
nonheparinized animals. A p value of less than 0.05 was considered a
statistically significant difference.
Results
Statistical Analysis of Bleeding Amount
Table 1 presents the
bleeding amounts and the laboratory results of the 11 dogs we studied.
Heparinization (at 300 U/kg) markedly prolonged the activated partial
thromboplastin time (42.7 ± 8.0 [SD] sec). In the nonheparinized group,
the mean (± SD) volumes of blood loss after splenic biopsy were as
follows: control sites, 19.72 ± 10.61 g; radiofrequency cauterized
sites, 0.05 ± 0.07 g; Histoacryl-Lipiodol mixture plugged sites, 0.38
± 0.32 g; and biopsy tract embolized sites using absorbable gelatin
sponge, 0.17 ± 0.16 g. In the heparinized group, the mean volumes of
blood loss after splenic biopsy were for control sites, 102.53 ± 52.51
g; radiofrequency cauterized sites, 0.03 ± 0.05 g; Histoacryl-Lipiodol
mixture plugged sites, 46.33 ± 41.06 g; and biopsy tract embolized
sites using absorbable gelatin sponge, 8.08 ± 18.04 g. In both the
nonheparinized and heparinized groups (both: p < 0.0001, analysis
of variance), statistically significant differences in blood loss were
observed among control sites and sites that were administered one of the
postbiopsy bleeding reduction procedures.
Table 2 summarizes the
results of the Tukey-Kramer test for multiple comparisons of postbiopsy
bleeding amounts. In the nonheparinized group, all the postbiopsy bleeding
reduction procedures examined in this study showed a statistically significant
reduction in bleeding compared with the control procedure (p <
0.001), and no significant difference was observed in postbiopsy blood loss
for sites that received postbiopsy bleeding reduction procedures (p
> 0.05) (Table 2). In the
heparinized group, all postbiopsy bleeding reduction procedures statistically
reduced bleeding compared with the control procedure. Moreover, radiofrequency
cauterization (p < 0.01) and biopsy tract embolization using
absorbable gelatin sponge (p < 0.05) reduced bleeding
significantly more than application of the Histoacryl-Lipiodol mixture
(Table 2). However, no
significant difference was observed between radiofrequency cauterization and
absorbable gelatin sponge embolization in terms of bleeding amount (p
> 0.05).
Control and Histoacryl-Lipiodol mixture plugged sites in the heparinized
group bled more than those in the nonheparinized group with statistical
significance (p < 0.0001 and p = 0.0021,
respectively).
Procedure Time
The means of the procedure times required for radiofrequency cauterization,
splenic biopsy tract embolization using absorbable gelatin sponge, and
Histoacryl-Lipiodol mixture plugging were 25.4 ± 3.7 sec, 309.9
± 65.3 sec, and 22.7 ± 2.8 sec, respectively. Statistically
significant differences in procedure times were seen among the postbiopsy
bleeding reduction procedures (p < 0.0001, analysis of variance).
The Tukey-Kramer test for multiple comparisons of procedure times revealed
that gelatin sponge embolization was the longest procedure (p <
0.001).
CT Analysis
In all radiofrequency-cauterized biopsy tracts, ablated areas of low
attenuation without contrast enhancement were observed, suggesting the
presence of splenic parenchymal necrosis
(Fig. 4). Focal
Histoacryl-Lipiodol mixture collections at the plugged sites of the spleen
were observed in all dogs (Fig.
5) but no demonstrable CT findings were observed at absorbable
gelatin sponge embolized sites.
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Fig. 4 —Axial contrast-enhanced portal venous phase helical CT scan
obtained 3 days after radiofrequency cauterization of splenic biopsy site
shows unenhanced splenic area (arrow), which suggests necrosis.
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Fig. 5 —Axial unenhanced helical CT scan obtained 3 days after
Histoacryl-Lipiodol (tissue adhesive, B. Braun-iodized oil, Guerbet) mixture
plugging of splenic biopsy site shows Histoacryl-Lipiodol mixture with high
attenuation (arrow) in spleen.
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In all dogs, no evidence of delayed postbiopsy bleeding was noted at the
splenic biopsy sites on CT. Multiple Histoacryl-Lipiodol mixture emboli were
seen on follow-up CT in the splenic and portal veins in all dogs
(Fig. 6).
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Fig. 6 —Portal venous phase CT scan with 3D reconstruction using 3D
software program (Rapidia, Infinitt) shows multiple Histoacryl-Lipiodol
(tissue adhesive, B. Braun-iodized oil, Guerbet) mixture emboli in portal vein
(arrows) and splenic vein (arrowhead). Multiple bright dots
in liver with no annotation are also portal emboli.
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Discussion
Because of the vascularity and inaccessibility of the spleen,
interventional radiologists have been particularly concerned about the risk of
hemorrhagic complications related to splenic biopsy
[9]. In cancer patients with a
splenic lesion, fine-needle aspiration biopsy has a major complication rate of
as much as 9.1%, but the reported diagnostic yields of splenic fine-needle
aspiration using 22- or 23-gauge needles vary from 15% to 100%
[5-8].
Recently, sonographically guided splenic core biopsy has been reported in the
literature as a simple and well-tolerated technique for acquiring splenic
tissue for diagnosis, staging, and follow-up of malignant lymphomas
[2,
3] and for determination of
splenic disease in patients with parenchymal abnormalities
[3,
9]. In patients with suspected
splenic involvement by lymphoma, better diagnostic accuracy of tissue core
needle biopsy (90.9%) than of fine-needle aspiration (68.5%) was reported by
Civardi et al. [18]. However,
Lindgren et al. [3] experienced
four major complications among 32 patients (13%) examined by splenic core
biopsy. All four patients had severe bleeding requiring transfusion, and one
required splenectomy. Lucey et al.
[11] also reported that three
patients required emergency splenectomy after a splenic core biopsy. Because
some splenic biopsies are performed in immunosuppressed patients or in
relapsed malignancies, there is a substantial clinical need to identify
effective techniques for reducing postbiopsy bleeding and related major
complications in the spleen. Despite several methods to reduce bleeding after
liver or kidney biopsy using hemostatic agents such as absorbable gelatin
sponge, coil, fibrin sealants, a Histoacryl-Lipiodol mixture, or applied
radiofrequency energy [1,
12-17],
no study has evaluated the comparative performances of these methods for
post-biopsy bleeding control in the spleen.
In this study, we used three methods of postbiopsy bleeding reduction in a
dog model of splenic core biopsy—namely, radiofrequency cauterization,
splenic biopsy tract embolization using absorbable gelatin sponge, and
Histoacryl-Lipiodol mixture plugging. We artificially created a coagulopathic
state in six dogs (the heparinized group) by the IV administration of heparin.
In both the heparinized and nonheparinized groups, all postbiopsy bleeding
reduction procedures significantly reduced bleeding at the biopsy site
compared with the controls. However, no significant difference in bleeding was
observed among these three bleeding control techniques in the nonheparinized
group. However, in the heparinized group bleeding was successfully increased
at the biopsy site. In this group, both radiofrequency cauterization in the
splenic biopsy tract and absorbable gelatin sponge tract embolization reduced
postbiopsy bleeding more than the control and Histoacryl-Lipiodol mixture
plugging procedures. In addition, heparin administration did not increase
postbiopsy bleeding in dogs that received radiofrequency cauterization or
biopsy tract embolization using the absorbable gelatin sponge method. Although
no significant difference in postbiopsy bleeding was observed between
radiofrequency cauterization and gelatin sponge embolization by the
Tukey-Kramer test, the procedure time of gelatin sponge embolization was
significantly longer than that of radiofrequency cauterization.
Lee et al. [17] reported
that Histoacryl-Lipiodol mixture plugging, when used to plug the renal biopsy
tract, is an efficacious method to control bleeding. However, we found
multiple Histoacryl-Lipiodol mixture emboli in the splenic and portal veins on
follow-up CT. The transarterial administration of a Histoacryl-Lipiodol
mixture has a therapeutic effect on bleeding conditions such as those due to
gastric ulcer bleeding or a pseudoaneurysm associated with trauma. In these
cases, the Histoacryl-Lipiodol mixture is carefully administered using
selective angiography under fluoroscopic guidance. However, biopsy tract
embolization without producing an unexpected embolism is difficult when a
Histoacryl-Lipiodol mixture is used for postbiopsy tract embolization. Thus,
we believe that Histoacryl-Lipiodol mixtures are limited by the potential risk
of embolism when used for postbiopsy tract plugging.
Follow-up CT revealed splenic parenchymal necrosis at the radiofrequency
cauterization site but produced no remarkable findings at tract embolization
sites using absorbable gelatin sponge. Kim et al.
[19] also observed thermal
damage at the biopsy site due to direct electrocauterization. However,
although the needle tract seeding of a tumor is rare, it has been reported
[20,
21]. When seeding occurs, the
effects can be catastrophic if a resectable tumor becomes unresectable. Thus,
thermal ablation of the tract as the needle is removed could, in theory,
reduce the incidence of needle tract seeding
[1] because the high
temperatures required for tract ablation are likely to kill any malignant
cells introduced into the tract during biopsy
[1]. However, to our knowledge
this has not been verified, and therefore it remains unclear whether
radiofrequency ablation is more effective than embolization at preventing
tumor seeding. Moreover, a potential weakness of radiofrequency cauterization
and Histoacryl-Lipiodol mixture embolization is that the organ tissue at
biopsy sites is altered by the procedure, which potentially makes repeat
biopsies and histologic analysis at the exact site problematic
[1].
Our study has several recognized limitations. First, the cost-effectiveness
of radiofrequency cauterization, absorbable gelatin sponge embolization, and
Histoacryl-Lipiodol mixture plugging in the postbiopsy bleeding reduction was
not evaluated. Although the additional cost of radiofrequency cauterization
after needle biopsy is higher than that of other procedures, radiofrequency
cauterization has the benefits of effective bleeding control and a short
procedure time in postbiopsy bleeding reduction in both normal and
coagulopathic conditions. Second, technical failures of postbiopsy bleeding
control procedures, such as the effect of introducer sheath displacement or
vessel fenestration by the biopsy cutting needle, were not considered because
we performed the procedures and measured bleeding amount directly from the
surgically exposed spleen. In clinical application, biopsy tract embolization
using an absorbable gelatin sponge is presumed to have a greater chance of
technical failure than the other procedures because of the relatively longer
procedure time. Third, bleeding as measured during this study would tend to
underestimate bleeding in the clinical setting. However, we believe that this
is not a serious problem with respect to comparisons of bleeding between the
procedure groups.
In conclusion, radiofrequency cauterization, biopsy tract embolization
using absorbable gelatin sponge, and Histoacryl-Lipiodol mixture plugging are
all efficacious methods to control postsplenic biopsy bleeding. However,
Histoacryl-Lipiodol mixture plugging is limited by its propensity to cause
splenic and portal vein embolism, and gelatin sponge tract embolization needs
a comparatively long procedure time. Thus, although parenchymal alteration is
inevitable, radiofrequency cauterization offers the benefits of effective
bleeding control and a short procedure time.
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Abstract
Introduction
