42 The Canadian Journal of Veterinary Research 2009;73:42–48
Laparoscopic surgery to obtain kidney biopsy samples in sup-
port of drug residue elimination profile studies in steers has been
described for gentamicin and penicillin (1,2). Pharmacokinetic corre-
lation studies of fluids and tissues depend on simultaneous sampling
of the fluids and tissues. Rapid, nontraumatic, minimally invasive
sampling techniques are a fundamental necessity in the successful
completion of tissue–fluid pharmacokinetic correlation studies.
Laparoscopy-guided liver biopsy with CO2 insufflation has
been performed in large animals under general anesthesia (3) and
in standing horses (4). Liver biopsy is widely used for obtain-
ing liver samples from living animals, and repeated observa-
tions can be made on the same animal (5). Endoscopy-guided
serial liver biopsy has been described in recumbent sheep (6).
Under laparoscopy the liver can be observed directly, an optimal
biopsy site can be selected, and the site can be monitored for
hemorrhage (7). Obtaining liver biopsy samples by laparoscopy
has been referenced in the standing horse (4) but has not been
reported in the standing bovine. This article describes in detail
the laparoscopic liver biopsy procedure as performed in standing
Isobaric (gasless) laparoscopic liver and kidney biopsy in standing steers
O. Alberto Chiesa, Jurgen von Bredow, Hui Li, Michelle Smith
The purpose of the current study was to investigate the suitability of an isobaric laparoscopic procedure, using a single port, for
obtaining serial kidney and liver biopsy samples from standing steers. The samples were used in support of a pharmacokinetic
tissue–fluid correlation study. Laparoscopic access was performed 3 times in each of 8 healthy Holstein steers, alternating from
the right side to the left side and then to the right side again. The surgery was performed in standing stocks after the animals
were given 3 doses of sulfadimethoxine sulfate intravenously and fasted for at least 18 h. Sedation and analgesia were achieved
with acepromazine and xylazine. Lidocaine 2% was injected at the center of the paralumbar fossa (left or right), and an incision
was made for introduction of a trocar–cannula assembly. Room air was allowed to enter the abdomen through the cannula at
the time of insertion. Once the peritoneal cavity was reached, an operating endoscope was inserted. No pressurized insufflation
was performed. A biopsy forceps was introduced into the operating channel of the endoscope to obtain a 100-mg kidney or liver
sample. No complications were encountered. The 24 laparoscopic procedures provided 24 kidney and 16 liver samples. The
results suggest that the isobaric (gasless) single-port laparoscopic technique is feasible for kidney and liver biopsy on standing
steers. The procedure can be performed in a reliable and efficient manner in the sedated standing bovine.
L’objectif de la présente étude était d’étudier la pertinence d’une procédure isobare de laparoscopie, utilisant une entrée unique, pour
obtenir des biopsies rénales et hépatiques en série chez des bouvillons en position debout. La procédure de biopsie a été utilisée pour fournir
des échantillons de rein et de foie dans le cadre d’une étude pharmacocinétique de corrélation tissu-fluide. L’accès par laparoscopie a été
effectué trois fois chez chaque animal en alternance du côté droit au côté gauche et de retour au côté droit. La chirurgie par laparoscopie a
été effectuée en position debout après que les animaux eurent reçus du sulfate de sulfadimethoxine et mis au jeûne pour au moins 18 heures.
La sédation et l’analgésie se sont faites par administration d’acépromazine et de xylazine. De la lidocaïne 2 % a été injectée au centre de la
fosse paralombaire (gauche ou droite) et une incision faite afin de permettre l’introduction d’un ensemble trocart-canule. Au moment de
l’insertion, on permit à l’air ambiant de pénétrer dans l’abdomen à travers la canule. Une fois le péritoine atteint, l’endoscope opératoire
a été inséré et aucun gonflement n’a été effectué. Un forceps à biopsie a été introduit dans le canal opératoire de l’endoscope afin d’obtenir
un échantillon de 100 mg de rein ou de foie. Aucune complication n’est survenue. Vingt-quatre procédures de laparoscopie ont fourni
24 échantillons de rein et 16 échantillons de foie à partir d’un total de 8 bouvillons. L’évaluation de 24 procédures de laparoscopie sur huit
bouvillons Holstein en santé suggère que la technique de laparoscopie isobare (sans gaz) avec une entrée unique est réalisable pour obtenir
des biopsies de foie et de rein sur des bouvillons en position debout. La procédure peut être réalisée d’une manière fiable et efficiente chez des
bovins sous sédation en position debout.
(Traduit par Docteur Serge Messier)
Center for Devices and Radiological Health, Office of Science and Engineering Laboratories, Division of Biology, Laboratory of Cardiovascular
and Interventional Therapeutics, Food and Drug Administration, 8401 Muirkirk Road, Laurel, Maryland 20708, USA (Chiesa); Center for
Veterinary Medicine, Office of Research, Division of Residue Chemistry, Food & Drug Administration, 8401 Muirkirk Road, Laurel,
Maryland 20708, USA (von Bredow, Li, Smith).
Address all correspondence to Dr. O. Alberto Chiesa; telephone: (301) 210-4248; fax: (301) 210-4685; e-mail: firstname.lastname@example.org
Received October 30, 2007. Accepted April 11, 2008.
2000;64:0–00 The Canadian Journal of Veterinary Research 43
Laparoscopic kidney biopsy with the use of CO2 insufflation has
been described in bovines (8–10). The procedure in the standing
steer has improved from the 2-port technique (8), to the 1-port tech-
nique (10), and ultimately to the isobaric (gasless), 1-port surgical
technique reported here.
Insufflation of CO2 into the peritoneal cavity is a routine technique
for abdominal exposure in laparoscopic surgery (11–15). The insuf-
flation system is used to create pneumoperitoneum (distention of the
peritoneal cavity with some type of gas), which improves visualiza-
tion and facilitates instrumental and visceral manipulation during
surgery (16). In standing laparoscopy in the bovine, gas insufflation
of the peritoneal cavity can produce discomfort, restlessness, and
even collapse in prolonged examination periods (14,17). Signs of colic
are evident in standing cows when the intra-abdominal pressure
exceeds 10 mmHg (18). If the patient moves extensively, damage
to laparoscopic equipment and contamination of the abdomen due
to loss of aseptic technique can result (14). During standing laparo-
scopic surgery, cattle frequently simply lie down when the abdomen
is inflated. The discomfort produced by the elevated pressure in the
peritoneal cavity may be avoided by lack of gas insufflation.
We performed isobaric (gasless) laparoscopic kidney and liver
biopsy in standing steers to evaluate the utility of this approach to
obtaining serial kidney and liver samples in standing steers.
Materials and methods
This study was approved by the Institutional Animal Care and
Use Committee, Office of Research, Center for Veterinary Medicine,
US Food and Drug Administration, and was conducted in accor-
dance with the guidelines provided by the US Animal Care and
Use of Laboratory Animals, in climate control facilities approved
by the American Association for the Assessment and Accreditation
of Laboratory Animal Care.
The study group comprised 8, clinically normal and drug-naïve
Holstein steers, aged 4 to 6 months, and ranging in weight from
193 to 330 kg. Each animal was housed separately in a temperature-
controlled barn with an automated lighting cycle. The animals were
fed mixed standard feed once daily. Hay and water were available
at all times.
The steers were enrolled in a pharmacokinetic study to monitor
the depletion of sulfadimethoxine in tissues and biologic fluids.
A complete blood profile (ruminant profile) and a clotting profile
were obtained before drug administration. Values out of normal
range in either profile would have excluded an animal from the
study. The steers were given the drug intravenously in an approved
3-dose regimen: 55 mg/kg followed by 2 doses of 27.5 mg/kg at
In 1 group of 4 animals, kidney and liver biopsy specimens were
obtained at 36, 60, and 84 h after the final dose of sulfadimethoxine.
In the remaining group of 4 animals, the samples were obtained
at 60, 84, and 108 h after the final dose of sulfadimethoxine. Thus,
in each animal, biopsy samples were obtained 3 times, with a 24-h
interval between each laparoscopy. The animals were slaughtered
6 h after the last biopsy, and necropsy was performed.
The surgical procedure was performed by 1 surgeon in sterile
dress with a nonsterile assistant.
Equipment — Standard laparoscopy instruments included the
following: 300-W xenon light source; 4.8-mm-diameter optic light
cable; 57-cm-long, 10-mm-diameter, rigid endoscope providing a
30° view; 27-cm-long, 10-mm-diameter, 0° rigid operating telescope
with a 6-mm-diameter instrument channel and parallel eyepiece;
20-cm-long, 11-mm-diameter cannula with a blunt trocar; atraumatic
forceps; and laparoscopic curved serrated scissors 40-cm long with
a 5-mm outer diameter. Blakesley biopsy forceps 5 mm in diameter
and 43 cm long were used to obtain all biopsy specimens. The endo-
scope contained a 6-mm-diameter working channel for insertion of
5-mm-diameter laparoscopy instruments (scissors, biopsy forceps,
grasping forceps). All equipment was purchased from Karl Storz
America, Goleta, California, USA.
Animal preparation and anesthesia — The steers were fasted for at
least 18 h before surgery. Immediately before surgery they were hal-
tered, led into a stock, and loosely restrained to minimize movement.
An intramuscular injection of acepromazine (acepromazine maleate
injection, 10 mg/mL; Boehringher Ingelheim, St. Joseph, Missouri,
USA), 0.025 mg/kg, was then administered. The paralumbar fossa
(either right or left) was clipped, shaved, scrubbed with povidone
iodine, and rinsed with alcohol. An intravenous catheter was asepti-
cally placed in the left jugular vein for the administration of xylazine
(Sedazine, diluted 1/100 in sterile saline solution; manufactured for
Fort Dodge Animal Health, Overland Park, Kansas, USA, by Phoenix
Scientific, St. Joseph, Missouri, USA), 0.005 to 0.01 mg/kg. As soon
as the animal was adequately sedated, it was covered with a sterile
drape. Next, 12 mL of lidocaine (2% lidocaine injectable, 20 mg/mL;
Bimeda Animal Health, Riverside, Missouri, USA) was infiltrated
in the center of the paralumbar fossa at the proposed incision site.
A 2-cm-long incision was made through the skin with a #22 surgery
blade, and blunt dissection was done with Metzenbaum scissors
through the muscles to facilitate insertion of the trocar cannula.
Isobaric right-flank laparoscopy (for access to the right kidney
and right liver lobe) — The trocar cannula was inserted perpen-
dicular with a rotating movement through the skin incision. When
resistance was met, the trocar assembly was thrust into the peritoneal
cavity, with the point directed slightly cranial and 45° to the lateral
body planes. The air valve on the trocar cannula was kept open,
and a rush of air was audible as the peritoneum was perforated.
The blunt trocar was then replaced with the endoscope, which
was inserted in the same direction as the trocar assembly had been
inserted. The endoscopic field was over the great omentum. The
endoscope was guided craniomediodorsally until the liver was in
view on the screen. A rapid examination was performed to ensure
a lack of trauma. The endoscope was then replaced by the operat-
ing telescope, which was directed to the upper right quadrant for
observation of the anatomic landmarks needed for the liver biopsy:
right triangular ligament, quadrate lobe, right kidney (embedded in
a large amount of perirenal fat, termed the “adipose capsule”), and
diaphragm (Figure 1). At the end of the procedure the endoscope was
44 The Canadian Journal of Veterinary Research 2000;64:0–00
removed and the skin incision closed with a single interrupted suture
(2-0 Monosof USS DG nylon polyamide; United States Surgical, a
division of Tyco Healthcare Group, Norwalk, Connecticut, USA).
The second laparoscopic incision on the right side was made 2.5 cm
caudal to the first incision.
Isobaric left-flank laparoscopy (for access to the left kidney) —
The trocar was similarly introduced and directed caudally through
the left paralumbar fossa toward the right coxofemoral joint. Once in
the peritoneum (as determined by an audible rush of air), the trocar
was replaced with the endoscope, which was guided cranially to the
upper left quadrant. The dorsal sac of the rumen was gently pushed
down with the endoscope, and the left kidney emerged on the screen
(Figure 2). The anatomic structures identified were the dorsal sac of
the rumen, the left kidney, and the psoas muscle. At the end of the
procedure the endoscope was removed and the skin incision closed
with a single interrupted suture (2-0 Monosof USS DG nylon poly-
amide, United States Surgical).
One-port liver biopsy technique — Two liver biopsy samples were
obtained from the ventral margin of the right lobe approximately
2 cm apart. The first sample was taken ventral, the second sample
(taken immediately afterwards) dorsal (Figure 3). The ventral margin
was observed directly with the endoscope to monitor for hemorrhage
at the biopsy site.
One-portal kidney biopsy technique — Upon completion of the
liver biopsy, the endoscope was redirected dorsally in preparation
for the kidney biopsy sample. With a curved serrated scissors, intro-
duced into the operating channel of the endoscope, the capsule of
the kidney was dissected in a cross pattern by rotating the scissors
90° after the first cut, and then a biopsy sample was obtained with
Blakesley biopsy forceps introduced through the operating channel
into the cross incision in the capsule.
A grasping forceps was used to control hemorrhage. The cut edges
of the kidney capsule were compressed for at least 2 min. The endo-
scope and grasping forceps were left in situ until it was possible to
verify that hemorrhage was controlled.
Data acquisition — Each laparoscopic procedure was fully
recorded by means of a Sony medical image system on an individual
compact disc. After completion of the procedure, the recording was
reviewed by the investigators, who recorded biopsy time, number
of punched “bites” per sample, and degree of hemorrhage (8). The
liver biopsy time was defined from when the endoscope was placed
in the peritoneum until the last liver sample was taken. The right
kidney biopsy time was defined from when the endoscope reached
the right kidney, until the endoscope was withdrawn from the peri-
toneal cavity. The left kidney biopsy time was defined from when
the endoscope was placed in the peritoneum until it was withdrawn
from the peritoneal cavity.
Post-operative management — The animals were transported
to the barn in a trailer towed by a tractor immediately after the
Figure 2. Isobaric (gasless) laparoscopic view of the left paralumbar
approach. R — rumen dorsal sac; LK — left kidney; PM — psoas muscle.
Figure 3. Minimal hemorrhage is observed after liver biopsy. The longer
arrow indicates the second biopsy site and the shorter arrow the first
Figure 1. Isobaric (gasless) laparoscopic view of the right paralumbar
approach. The important anatomic landmarks for liver biopsy are: right
kidney, right triangular ligament (RTL), quadrate lobe of the liver (QL), right
lobe of the liver (RL), and diaphragm (D). Yellow circle — biopsy site.
2000;64:0–00 The Canadian Journal of Veterinary Research 45
surgery. Once in their pen, the steers were allowed free access
to hay, feed, and water. Respiratory rate, heart rate, tempera-
ture, appetite, attitude, and postural positions were evaluated and
recorded 4, 8, 12, and 24 h after surgery or until the animal was
slaughtered. No special care was given to any steer, and no antimi-
crobial or antinflammatory agent was administered. A sweet treat
(100 to 200 g of Omolene, Purina Mills, St. Louis, Missouri, USA)
was given at the time of each evaluation to encourage coopera-
tion and avoid stress. The surgical incision site was inspected for
The steers were humanely killed by captive bolt stunning and
exsanguination 6 h after the last biopsy. Immediately after slaughter,
both kidneys and the liver were removed. The kidneys were cleaned
of surrounding fat and the capsules dissected to enable inspection
of the kidney surface. The biopsy areas and surrounding tissue were
carefully explored in the liver and kidney.
Of the 24 laparoscopic surgical procedures performed on the
8 standing steers, 16 were performed on the right side (which
provided 16 kidney and 16 liver samples) and 8 (which provided
8 kidney samples) were performed on the left. Laparoscopic access
was achieved in all cases, and no complications were encountered.
The animals showed no signs of ataxia, distress, or discomfort during
the procedures; they remained quiescent and did not interfere with
placement of the laparoscopic instruments by moving. No complica-
tions were observed in any of the animals after the surgery or during
transportation to the barns.
Liver results — An acceptable liver sample consisted of 2 or
more biopsy bites (mean number 2.2). The mean liver biopsy time
was 1.5 min. The mean sample weight was 119.2 mg. Data for the
individual animals are provided in Table I. At the time of the second
biopsy (48 h after the first), no significant tissue alterations were
observed at first biopsy with the endoscope.
Right kidney results — Each tissue sample consisted of at least
2 biopsy bites (mean number 2.2). The mean biopsy time was 4.6 min.
The mean sample weight was 113.9 mg. All procedures showed mod-
erate hemorrhage at the biopsy site (8). Bleeding was controlled with
the application of pressure with forceps for 2 min. All samples were
classified as easy to obtain: “no complications, easily recognizable
kidney surface, easy to obtain biopsy”(8).
Table I. Results of serial kidney and liver biopsy in 8 standing Holstein steers
Number of biopsy
bites per sample
Biopsy time (minutes)
Sample weight (mg)
46 The Canadian Journal of Veterinary Research 2000;64:0–00
Left kidney results — Each tissue sample consisted of at least
2 biopsy bites (mean 2.6). The mean biopsy time was 4.6 min. The
mean sample weight was 126.1 mg. The kidney surface was easily
detected, and all samples were classified as easy to obtain. Applying
pressure with forceps for 2 min stopped hemorrhage.
Postmortem results — No adhesions, infections, or gross changes
were detectable in any of the steers’ carcasses when the kidneys and
the liver were harvested. The biopsy sites were clearly visible in the
kidney cortex and very easy to identify in the right lobe of the liver.
No hemorrhage at the biopsy bite site or in the abdominal cavity
was found in any of the 8 steers.
Drug analysis — All the samples obtained by laparoscopy were
of sufficient weight for sulfadimethoxine analysis.
Laparoscopic surgery presents the surgeon with the problem of
working within a confined space. In both human and animal surgery,
a routine technique is to expand this working space by elevating the
internal abdominal pressure. Expansion of the space improves the
surgeon’s view of the internal organs and facilitates manipulation
of the surgical instruments.
For most laparoscopic procedures gas insufflation to create suf-
ficient visual and operating space is mandatory (13); however,
gas insufflation, especially over prolonged examination periods,
produces animal discomfort and restlessness and may even result
in the animal’s collapse (17). The animal may experience some
postoperative discomfort related to the use of CO2 (12), which has
been reported to form carbonic acid on the moist peritoneal surface
in humans (19,20).
Recent evidence suggests that the use of CO2 to create pneumo-
peritoneum during laparoscopy can lead to structural, metabolic,
and immune derangements within the peritoneal cavity that include
structural alterations in the mesothelial lining, pH disturbances, and
alterations in peritoneal macrophage responsiveness (21).
The effect of CO2 insufflation has been studied in llamas (22), horses
(23), ewes (24), dogs (25), and pigs (26). There are no reports that dis-
cuss the secondary effect of CO2-induced pneumoperitoneum or ambi-
ent air in cattle (27); however, signs of colic are evident in standing
cows when the intra-abdominal pressure exceeds 10 mmHg. (18).
Because of the adverse physiological effects and technical disad-
vantages of pneumoperitoneum, alternative methods of abdominal
wall lifting have been explored (28–30). It has been reported that
with isobaric (gasless) laparoscopy the adverse effects and potential
risk of CO2 insufflation are eliminated; post-operative convalescence
is improved, and post-operative pain reduced (31).
Our investigation attempted to simplify the laparoscopic biopsy
technique by avoiding pressurized CO2 insufflation. Even though our
goal was not to evaluate the effect of CO2 on laparoscopic surgery,
we believe that the standing steer could be a good model for compar-
ing procedures performed with and without CO2 insufflation. The
current study has refined and improved the standard 2-port and the
1-port techniques discussed previously (8,10). These improvements
enable safe sampling with minimal or no postsurgical recovery time,
which allows more frequent sampling to provide a greater number
of samples throughout the drug residue elimination phase.
The isobaric approach is possible in the standing steer since
pneumoperitoneum occurs by the incorporation of room air through
In the standing steer, the posterior portion of the rib cage and the
dorsal ligaments form a semisolid structure from which the kidneys
and the liver are suspended. The suspension and the aspiration of
some room air provide space between the organs and allow the
organs to be approached laterally, so that biopsy may be done with-
out the usual CO2 insufflation to create additional space. The natural
“tenting” effect is probably only possible in the sedated large stand-
ing animal. However, a similar effect may be possible with proper
positioning of the anesthetized patient. The lack of discomfort and
the rapid recovery after surgery may be attributed to the lack of gas
insufflation throughout this study.
Isobaric (gasless) laparoscopy allows the use of conventional
laparotomy instruments and reduces operative time and cost (32).
No gas seal is necessary to maintain the intra-abdominal pressure,
and no technical assistance is needed to control CO2 flow through-
out the procedure. The cost of CO2 insufflation and the associated
equipment is eliminated. The current isobaric, 1-port procedure can
be performed by a single surgeon.
It has been reported that care should be taken before performing
laparoscopy in an animal with gastrointestinal distention (33). In
the bovine, a 24-h fast is necessary to decrease ruminal and other
visceral volume sufficiently to allow successful laparoscopy (14).
In the current study, an 18-h fast was enough to decrease visceral
volume and allow access.
In human medicine, renal biopsy is considered the diagnostic
procedure of choice for many patients in whom renal disease is
suspected (34). Ultrasound-guided percutaneous biopsy has recently
been described in cattle (35). The authors stated that the risk of seri-
ous complications was very low. The reported approach provided
access to only the right kidney; the left kidney could not undergo
biopsy during ultrasound visualization.
Hemorrhage after ultrasound-guided biopsy of the kidneys has
been reported in small animals (36). Laparoscopy provides excellent
visual control for positioning the biopsy forceps, provides for the
application of pressure to the biopsy site, and allows monitoring
for hemorrhage after the biopsy (37). The learning curve for the
ultrasound-guided procedure was steeper than that for laparoscopic
Hemorrhage from liver biopsy is a particular concern in animals
with liver disease because hepatic dysfunction may cause concurrent
coagulopathy (7). No prolonged hemorrhage was observed in the
healthy animals in the current study.
When kidney and/or liver samples are collected in support of
pharmacokinetic studies, repeated sampling of the same animal at
various times provides greater consistency than single-time sampling
of a greater number of animals. The reduction of animal-to-animal
variation through the use of serial sampling to monitor drug residue
depletion in only a few animals has been discussed previously (1,2)
and can be maintained with the current isobaric procedure.
We performed the single-port isobaric procedures with the pur-
pose of obtaining serial liver and kidney samples with minimal
discomfort to the animal. The results indicate that laparoscopic
biopsy performed through a single port without pressure insufflation
2000;64:0–00 The Canadian Journal of Veterinary Research 47
is both safe and cost-effective. Stress to the animal is kept at a
minimum, allowing multiple samples to be obtained from the same
animal within short intervals without distressing the animal. Serial
sampling of kidney and liver tissue in the same animal provides
ideal support for pharmacokinetic drug distribution and elimination
In clinical practice, isobaric liver or kidney biopsy could be useful
when a diagnostic procedure is needed to determine the severity of
a lesion and to formulate an optimal treatment plan.
The authors acknowledge the assistance of Ken Godden and
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