Veterinary Surgery

33:668–672, 2004

Evaluation of a Sheep Laparoscopic Uterine Trauma Model and

Repeat Laparoscopy for Evaluation of Adhesion Formation and
Prevention with Sodium Carboxymethylcellulose

JENNIFER M. EWOLDT, DVM, MS, DAVID E. ANDERSON, DVM, MS, Diplomate ACVS,
JOANNE HARDY, DVM, PhD, Diplomate ACVS, and STEVEN E. WEISBRODE, VMD, PhD, Diplomate ACVP

Objective—To evaluate topical application of 1% sodium carboxymethyl cellulose (SCMC) for

prevention of postoperative adhesions in a laparoscopic model of uterine trauma in sheep.
Study Design—Experimental study.
Animals—Fourteen non-pregnant ewes.
Methods—Ewes were randomly assigned to 1 of 2 groups: control (saline solution) or 1% SCMC
treatment. By left flank laparoscopy, traumatic forceps were used to create serosal trauma
(1.5
5 cm) and hemorrhage on the left uterine horn. Either 30 mL saline solution or 30 mL 1%
SCMC was applied topically to the traumatized uterine horn. Adhesion formation was evaluated by
repeat laparoscopy at days 14 and 21. Sheep were euthanatized on day 28 for necropsy evaluation of
adhesions.
Results—Five control sheep had adhesions of the uterine horn by day 14, but only 4 had adhesions
at day 21, and 2 at day 28. Adhesions did not occur in SCMC-treated sheep. No adhesions occurred
elsewhere in the abdomen.
Conclusions—Laparoscopically created uterine trauma is an effective method for induction of
uterine adhesions, and laparoscopy is an excellent method for serial evaluation of adhesion for-
mation. SCMC (1%) was effective at preventing adhesion formation in sheep and no inflammatory
response was noted.
Clinical Relevance—SCMC (1%) should be considered for prevention of adhesions in abdominal
surgery in sheep.
r Copyright 2004 by The American College of Veterinary Surgeons

Key words: uterus, serosal abrasion, adhesions, laparoscopy, sodium carboxymethyl cellulose, sheep.

INTRODUCTION tinal surgery; the incidence of clinically significant

adhesions is 14–22%.2–4 In foals surviving abdominal

A DHESIONS RESULT from an imbalance between

fibrin formation and fibrinolysis.1 Postsurgical ad-
hesions develop during normal healing after serosal in-
jury or ischemia and may be beneficial but can also result
in postoperative morbidity. In horses, postsurgical ab-
dominal adhesions are most common after small intes-
surgery, adhesions occurred in 19 of 90 foals, but only
resulted in clinical signs in 9 foals.5 Adhesions are re-
portedly the 2nd most common reason for repeat la-
parotomy in horses after colic surgery.6
In human surgery, adhesions involving the reproduc-
tive tract are of importance and appear to result from

From the Departments of Veterinary Clinical Sciences and Veterinary Biosciences, The Ohio State University, Columbus, OH.
Funded in part by a Surgeon-In-Training Research Grant from the American College of Veterinary Surgeons. This study comprised a
portion of the work for Dr. Ewoldt’s Master’s thesis at the Ohio State University, June 2002.
Dr. Hardy’s current address is College of Veterinary Medicine, Texas A&M University, 4475 TAMU, College Station, TX 77843-
4475.
Address reprint requests to: Dr. Ewoldt, Risius & Associates Veterinary Service, 112 E LeClaire Road, Eldridge, IA 52748.
Submitted January 2004; Accepted July 2004
r Copyright 2004 by The American College of Veterinary Surgeons

0161-3499/04
doi:10.1111/j.1532-950X.2004.04090.x
668
 EWOLDT ET AL
inflammation in, or surgery of, other areas of the abdomen.
Preservation of fertility in women during abdominal sur-
gery is of prime concern to human surgeons.7 In humans,
laparoscopic surgery resulted in a shorter hospital stay, less
postoperative discomfort, and more rapid return to normal
activity8; however, laparoscopy had an unexpectedly higher
incidence of adhesions than did laparotomy.9
Few studies have compared laparoscopic-induced peri-
toneal trauma to laparotomy-induced trauma, and none
in large animals. In rats, scissor cuts into the serosal sur-
face of the uterine horn resulted in a similar incidence of
adhesions by laparoscopy (17 of 31 rats) as with laparo-
tomy (18 of 30 rats).10 In dogs, a significantly larger sur-
face area of adhesions was seen after cecal resection by
laparotomy, compared with laparoscopy.11 In sheep, lap-
aroscopy alone resulted in little adhesion formation or
inflammatory response.12,13 Thus we selected lap-
aroscopic creation of adhesions in sheep because any ad-
hesion formation should reflect the induced injury rather
than laparoscopic technique.
Sodium carboxymethylcellulose (SCMC) is a surface
lubricant with high viscosity.14,15 It has 2 beneficial effects
in abdominal surgery: protective lubrication if applied
before abdominal exploration, and a hydroflotation ef-
fect, preventing surfaces from direct contact with each
other. SCMC is used in equine colic surgery,1,16 but has
not found favor in human surgery where dextrans and
barriers are preferred.7 SCMC is distributed throughout
the abdomen, unlike locally applied barriers, and there-
fore may help prevent remote adhesions, especially in the
ventral region of the abdomen once the patient is in a
standing position. However, because of gravitational ef-
fects, SCMC may not be as effective for the dorsally lo-
cated reproductive tract in a standing animal.
Instillation of 1% SCMC (1–2L) reduced adhesions in
ewes after laparotomy alone and significantly reduced
adhesion formation after uterine trauma.15 SCMC (1%;
1–2L) significantly reduced adhesions in horse models
including abrasion and resection of jejunum without ad-
versely affecting healing.14,17,18
We hypothesized that local application of 1% SCMC
would reduce postoperative adhesions in a laparoscopic
model of uterine trauma in sheep. Our first objective was
to evaluate a laparoscopic method for creation of uterine
trauma, and for serial evaluation of adhesion formation
in the abdominal cavity. Our second objective was to
evaluate small volume topically applied 1% SCMC for
prevention of uterine adhesions after uterine trauma.
MATERIALS AND METHODS
Animals
Fourteen adult non-pregnant female sheep with an un-
known reproductive history were obtained from a local farm.
669
Sheep were housed in groups (4–6) in bedded stalls, fed grass/
alfalfa hay ad libitum, and were acclimated for  4 days
before use. Sheep were examined for general physical health
and by ultrasonography for pregnancy. An assistant randomly
assigned sheep to treatment groups.
Observations from a Preliminary Study
We determined that single bolus intravenous (IV) an-
esthesia was adequate because the procedure was short and
could be completed before signs of recovery from anesthesia.
Endotracheal tubes were not used to prevent regurgitation
because the sheep were positioned in sternal recumbency, with
the head lowered. Sheep ate readily within hours of laparos-
copy, had no signs of pain or discomfort, so postoperative
analgesia was not administered.
Adhesion Model
Feed was withheld for 24 hours to reduce abdominal
visceral size and the possibility of regurgitation during sur-
gery. Before surgery, a blood sample was collected for a com-
plete blood cell count and fibrinogen concentration. To
eliminate inter-surgeon variation, 1 surgeon performed all
procedures.
Each sheep was anesthetized (0.05 mg/kg xylazine, 0.05 mg/
kg butorphanol, and 2 mg/kg ketamine IV) and positioned on
a surgery table in sternal recumbency in a modified Trend-
elenburg position with the hindquarters elevated. After aseptic
preparation and draping of a clipped left flank, a blunt trocar
and 10 mm laparoscopic cannula were inserted in the mid-
paralumbar fossa through a stab incision. After laparoscopic
observation of the viscera, the abdomen was insufflated (CO2;
insufflation pressure, 15–18 mm Hg). Insufflation pressure was
lowered if sheep had signs of difficulty breathing, but not to an
extent that impaired observation. A 2nd 10 mm cannula was
inserted in the paralumbar fossa, 3–5 cm caudoventral to the
1st portal, as an instrument portal.
The abdomen was explored for existing adhesions to the
uterus or visible organs. The left uterine horn was grasped
with an atraumatic laparoscopic forcep (10 mm Babcock
forcep, Karl Storz Veterinary, Goleta, CA). A 2nd instrument
portal was created 5 cm ventral to the 1st instrument
portal, and a traumatic forcep (10 mm Claw forcep, Karl
Storz) introduced to disrupt the serosa and subserosal sur-
face of the left uterine horn (1.5 cm
5 cm) and induce hem-
orrhage by complete closure of the forcep on the uterine horn
10 times.
The traumatized uterine horn was stabilized and 1 of the
treatments applied topically: either 30 mL saline (0.9% NaCl)
solution (control, n ¼ 8) or 30 mL 1% SCMC (n ¼ 6). After
treatment, the uterus was released, the abdomen decompressed
manually, and the portal incisions closed with suture incor-
porating the external abdominal oblique muscle and skin.
Sheep were recovered from anesthesia and returned to normal
feeding; no medications were administered after surgery.
670 SHEEP LAPAROSCOPIC UTERINE TRAUMA MODEL
Repeat Laparoscopic Evaluation
On days 14 and 21, sheep were anesthetized. A lap-
aroscopic portal was created in the left paralumbar fossa, and
if necessary, a 2nd portal was created to allow insertion of a
retractor to displace viscera. Presence or absence of adhesions
was noted, and the uterine trauma site observed to evaluate
healing. Care was taken not to disrupt any adhesions. Re-
sponse to uterine trauma (adhesion score) was graded subjec-
tively: 0 ¼ no evidence of tissue reaction; 1 ¼ fibrin deposition
(moderate to marked fibrin formation without adhesions);
2 ¼ adhesions.
Clinical Pathology
Venous blood samples were collected before each lap-
aroscopic procedure (days 0, 14, 21) and before euthanasia
(day 28) to determine complete blood cell count and fibrin-
ogen concentration, measured by nephelometry (IL/Coulter
ACL 7000, Miami Lakes, FL).
Necropsy Examination
On day 28, sheep were euthanatized and necropsied. Ad-
hesions were scored. Any adhesions were resected so that the
uterus could be removed as an entire organ which was pre-
served in 10% neutral buffered formalin.
Histopathology
A single longitudinal tissue section was obtained from each
uterine horn. If present, sites with adhesions or serosal defects
were included in sections otherwise sections were obtained
from the experimental region and a comparable region on the
other horn. Tissue sections were fixed in 10% neutral-buffered
formalin, embedded in liquid paraffin, and sectioned (5 mm)
before staining with hematoxylin–eosin. Sections were evalu-
ated for presence of white blood cells, fibroplasia, edema, and
adhesions. Histologic fibroplasia and inflammation were each
graded subjectively: absent ¼ 0, mild ¼ 1, or moderate ¼ 2.
Statistical Analysis
Descriptive statistics generated for blood analysis data and
laparoscopic adhesion scores were mean, median, standard
deviation, minimum, and maximum using a statistical pro-
gram (SAS version 8.01; SAS Institute Inc., Cary, NC). Data
sets were evaluated for normality using normal probability
plots. Data was analyzed by group and by day using ANOVA
(Proc Mixed, SAS version 8.01), using the Tukey–Kramer
procedure for multiple comparisons between groups. Adhe-
sion scores were compared between groups overall, as well as
by day, using Fisher’s exact test. A P-valueo.05 was con-
sidered significant for all tests.
RESULTS
Values for hematologic analyses were within normal
reference intervals for our hospital. In general, laparos-
copy and laparoscopic-induced uterine trauma were well
tolerated by sheep, and minimal systemic inflammatory
reaction occurred.
Adhesion Formation
Adhesions between the uterine horn trauma site and
omentum occurred in 5 control sheep by day 14. Serosal
fibrin deposition without adhesion formation was ob-
served in 1 other control sheep at day 14. At day 21, 4
control sheep had adhesions present (all of which had
adhesions at day 14), and only 2 of these sheep had ad-
hesions on necropsy at day 28. One control group sheep
died at day 18 and had peritonitis with diffuse adhesions;
this sheep had adhesions at day 14. Adhesions did not
occur in any of the treated sheep. Fibrin deposition was
observed in 2 SCMC sheep at day 14, but was not ap-
parent by day 21.
Adhesion Scores
There was a significant difference between control and
treated sheep for laparoscopic or necropsy adhesion
scores on days 14 and 21, but not on days 0 and 28
(Po.04; Table 1). Fisher’s exact test was significant for
overall differences in adhesion score between groups
(Po.0002).
Necropsy Observations
At necropsy, adhesions involving the uterine trauma
site were observed in 2 control sheep and none of the
SCMC. There were no adhesions at remote sites in any
sheep. Areas of previous trauma were visible as inden-
tations on the uterine horn surface, but these were com-
pletely covered by serosa in 12 of 14 sheep. In 1 control
sheep with adhesions, an abscess was observed near the
Table 1. Median Laparoscopic and Necropsy Abdominal Adhesion
Scores in Sheep after Topical Application of Saline Solution (Control) or
1% Sodium Carboxymethylcellulose (SCMC) to Injured Uterine sites
Adhesion Score
Time Control SCMC
Day 0 0a 0a
Day 14 2a 0b
Day 21 2a 0b
Day 28 0a 0a
Scores with different superscripts are statistically different (Po.04).
Scores were graded subjectively as 0 ¼ no adhesion, 1 ¼ fibrin deposition,
2 ¼ adhesion formation.
 EWOLDT ET AL
Table 2. Mean Fibroplasia and Inflammation Scores for Traumatized
and Contralateral Uterine Horns at 28 Days
Fibroplasia Score Inflammation Score
Traumatized Contralateral Traumatized Contralateral
Control 0.75 0.5 1.25 0.5
SCMC 0.33 0 0.5 0
Immediately after uterine trauma, topical application of saline solution
(control) or 1% sodium carboxymethylcellulose (SCMC) was used to
prevent adhesion formation. scores were subjectively graded 0 ¼ no reac-
tion, 1 ¼ mild reaction, 2 ¼ moderate reaction.
serosal surface and may have caused the extensive adhe-
sion formation and collagen deposition observed in that
animal.
Histologic Observations
Fibroplasia and inflammatory cell infiltration occurred
in 7 traumatized horns of control sheep, and 2 contra-
lateral horns. In SCMC sheep, 3 traumatized horns had
evidence of inflammatory reaction but none of the op-
posite horns. Fibroplasia and inflammation scores were
greater in the control group than in the treatment group,
for both traumatized and contralateral horns (Table 2),
however, differences were not significant.
Sections of adhesions had extensive fibrous connective
tissue on the serosal surfaces of the uterine horns, often
with associated influx of neutrophils, macrophages, and
other inflammatory cells. Disruption of serosal integrity
was seen in many locations on treated horns, sometimes
extending to subserosal muscular layer disruption. This
muscular disruption was believed from forcep bites dur-
ing the uterine trauma.
DISCUSSION
The laparoscopic uterine trauma model we used was
effective in inducing adhesions in sheep. Of 8 control
sheep, adhesions occurred in 5 and fibrin deposition in 1
sheep. This is a slightly lower percentage of adhesion
formation than reported for sheep after laparotomy15 or
in horses after laparotomy and serosal abrasion.19,20
Theoretically, compared with laparoscopy, laparotomy
would result in proportionately more tissue injury and
release of inflammatory mediators and thus cause in-
creased adhesion formation. Our laparoscopic model was
intended to study adhesion formation without the con-
founding factor of laparotomy, as well as observing how
many adhesions could be created by laparoscopy. We
successfully induced adhesions with laparoscopic trauma
to only 1 uterine horn in sheep and without formation of
remote adhesions.
671
Our sheep model is of particular interest for studies in
sheep and humans, because of a similar sized abdominal
cavity. Although anatomic relationships are quite differ-
ent, we believe that experimental techniques could be in-
itially tested on sheep, which reliably and repeatedly
produce abdominal adhesions after laparotomy15 or lap-
aroscopic trauma. Laparoscopic anatomy of sheep is
similar to that of cattle,21 but organs can be evaluated in
more detail because the abdominal cavity is smaller.
In these sheep, left flank laparoscopy allowed obser-
vation of the rumen, left liver lobes, uterus, bladder, both
kidneys, much of the small intestine, part of the spiral
colon and descending colon, and sometimes, part of the
right liver lobes. Withholding feed increased the regions
of the abdomen that could be examined. Sternal recum-
bency was used to minimize the likelihood of regurgita-
tion, to facilitate observation and manipulation of the
uterus, and to provide some gravitational stabilization of
the uterus.
Laparoscopy was excellent for serial evaluation of ad-
hesions without need for necropsy at different evaluation
times. In humans, repeat laparoscopy is used for evalu-
ation of adhesions after abdominal surgery and to per-
form early adhesiolysis.22 Repeat laparoscopy has been
reported in horses used for adhesion research.20,23 Repeat
laparoscopy was easy to perform and provided excellent
observation of viscera, particularly the uterus.
We avoided repeat laparoscopy until 14 days after in-
itial trauma because we did not want to disrupt early
fibrin deposition by insufflating the abdomen and sepa-
rating visceral surfaces. In humans and animals, fibrous
adhesions are formed within 7–14 days after trauma or
surgery, as fibroblasts migrate into fibrin on the serosal
surface.24 Thus we assumed that adhesions would be suf-
ficiently formed by 14 days to permit evaluation without
disruption. In 5 control sheep, adhesions had formed by
day 14, and no new adhesions formed after that time.
Interestingly, adhesions disappeared in 3 sheep by day 28,
so that only 2 sheep had adhesions at necropsy.
Although we were careful not to disrupt adhesions
during laparoscopy, it is possible that abdominal insuf-
flation did disrupt forming adhesions, as 3 adhesions
subsequently disappeared in the control group. However,
no freshly disrupted surfaces were seen during explora-
tion, which would suggest that something else caused the
adhesions to disappear. We assume that the fibrolytic
system in the abdomen was responsible.
One of the most interesting observations was that a
small volume (30 mL) of 1% SCMC was effective in pre-
venting adhesions to the traumatized uterus. Large vol-
umes (1–2 L) are typically used to prevent adhesion
formation in horses,16,17 and similar volumes have also
been used in sheep.15 One reason for use of large volume
SCMC was to provide a hydroflotation effect and phys-
672 SHEEP LAPAROSCOPIC UTERINE TRAUMA MODEL
ically separate viscera. However, 1–2 L SCMC seems in-
sufficient to provide hydroflotation in an equine abdo-
men, so we speculate a surface effect must occur at the
site of trauma. Certainly 30 mL (1% SCMC) would be a
very small volume in a sheep abdomen and unlikely to
result in physical separation of viscera. Our study pro-
vides evidence that smaller volumes of SCMC directly
applied to the region of interest at the time of trauma are
effective in adhesion prevention. Remote adhesions were
not observed. It is unknown if this was an effect of 1%
SCMC or attributable to minimally invasive surgery.
Adhesions to the laparoscope portals did not occur,
supporting human surgical evidence that these peritoneal
defects do not need to be sutured if they are small. A
small peritoneal defect is apparently insufficient to induce
adhesion formation, and skin sutures or deep muscle/
fascia sutures for closure of stab incisions appears suf-
ficient for closure.
We determined that laparoscopically created uterine
trauma was effective for creation of uterine adhesions in
sheep. Repeat laparoscopy was also useful for temporal
evaluation of presence of adhesions without the need for
large numbers of necropsies. Small volume (30 mL) 1%
SCMC was effective in preventing uterine adhesions after
laparoscopic uterine trauma.
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