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Efficiency of Omental Transposition on the Healing of Tibial Fracture in Dogs

Authors:
  • Faculty of Veterinary Medicine - University of Baghdad

Abstract

ABSTRACT The tibia is one of the slowest-healing bones in the body especially at the distal diaphyseal fracture, so the objective of this study, was to investigate the efficacy of omentum transposition on the healing of tibial fracture of the dogs. Ten healthy mongrel dogs were used in this experiment. Tibial distal third fractures were induced and immobilized by intramedullary pins. The animals divided into two equal group (n=5). The first group as a control groups (CG) and the second groups used omental transposition as treated groups (TG). Comprehensive studies were including lameness grade, functional outcome, radiographic evaluation and histopathological examination. The clinical result showed that the lameness grade was improved on immediate postoperative day in all TG animals and the functional outcome was graded as excellent in three cases (60.0%) and good in two cases (40%). Radiographs and histopathological sample have been taken for each group. On day 56 post operations, the radiological results of the treated group showed complete disappeared of fracture line, remodeling of fracture site and clinical union was evidenced by closure of fracture. Histological result showed that the treated group had highly vascularized, remodeling of trabecular bone, good appositional surfaces and active of endochondral ossification. The conclusion of study, it is appeared the omental pedicle enhancing healing of the distal third tibial fracture.
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Volume : 3 | Issue : 9 | Sept 2013 | ISSN - 2249-555X
RESEARCH PAPER
Microbiology
Efficiency of Omental Transposition on the Healing of
Tibial Fracture in Dogs
AL-Timmemi HA Ali A. Ajeel Kalid K. Kadhim
Surgary Department, Faculty of
Veterinary Medicine, Baghdad
University, Iraq
Surgary Department, Faculty of
Veterinary Medicine, Baghdad
University, Iraq
Anatomy Department Faculty of
Veterinary Medicine, Baghdad
University, Iraq
Al-Jashamy Karim
Pathology Department, Faculty of Medicine SEGI
University, Malaysia
Pathology Department, Faculty of Medicine SEGI
University, Malaysia
KEYWORDS
Tibia, Fracture, Omentum, Radiology, histology
ABSTRACT The tibia is one of the slowest-healing bones in the body especially at the distal diaphyseal fracture, so the
objective of this study, was to investigate the efficacy of omentum transposition on the healing of tibial frac-
ture of the dogs. Ten healthy mongrel dogs were used in this experiment. Tibial distal third fractures were induced and
immobilized by intramedullary pins. The animals divided into two equal group (n=5). The first group as a control groups
(CG) and the second groups used omental transposition as treated groups (TG). Comprehensive studies were including
lameness grade, functional outcome, radiographic evaluation and histopathological examination. The clinical result showed
that the lameness grade was improved on immediate postoperative day in all TG animals and the functional outcome was
graded as excellent in three cases (60.0%) and good in two cases (40%). Radiographs and histopathological sample have
been taken for each group. On day 56 post operations, the radiological results of the treated group showed complete
disappeared of fracture line, remodeling of fracture site and clinical union was evidenced by closure of fracture. Histological
result showed that the treated group had highly vascularized, remodeling of trabecular bone, good appositional surfaces
and active of endochondral ossification. The conclusion of study, it is appeared the omental pedicle enhancing healing of
the distal third tibial fracture.
Introduction
Tibial fractures account for the third most common type of
fracture after femur, radius and ulna (Seaman and Simpson,
2004), comprise 21.0 per cent (Unger et al., 1990) of all long
bone fractures. Tibial diaphyseal fractures account for 75.0%
to 81.0% of all tibial fractures (Boone et al., 1986). The goal
of any fracture treatment is to restore the anatomical shape
of the fractured bone to promote stability of fracture with
suitable implants and enable the limb to early ambulation.
The fracture repair techniques using bone plates, external
fixators, interlocking nails, intramedullary pins and external
coaptation are currently practiced in the tibial fracture man-
agement (Glyde and Arnett, 2006). During fracture healing,
new blood vessels sprout from existing blood vessels to re-
store blood supply and to facilitate bone regeneration. Inad-
equate bone vascularity is associated with decreased bone
formation and bone mass (Carano and Filvaroff, 2003). The
tibia is one of the slowest-healing bones in the body, prob-
ably because it seldom has a good hematoma from which
to form a callus. It is commonly that the distal diaphyseal
tibial fracture was healing more slowly (Piermatti and Flo,
1997), because the blood circulation to this part of the bone
is scanty (Leonard, 1971).
The omentum is a serious membrane made up of a lattice
of blood vessels and fat. It is composed of two mesothelial
sheets. It is ventrally attached to the greater curvature of
the stomach to the spleen and to the left lobe of the pan-
creas The omentum releases polypeptide growth factor and
activated macrophages, which results in capillary ingrowth
into surrounding tissue (Liebermann., 2000), because of the
omentum’s antimicrobial defense mechanisms and it has
ability to stimulate the neovascularization (Beelen, 1991),
lymphatic and angiogenic capacities (Singh et al., 2008).
Vascular endothelial growth factor (VEGF)-A of omentum
stimulates angiogenesis because it’s binding to VEGF re-
ceptors that promotes endothelial cell migration and prolif-
eration, which is required for the development of new blood
vessels (Ferrara, 2002). VEGF-A increases vascular permea-
bility that may contribute to angiogenesis. According to the
authors’ knowledge, this is the first experimental research,
in which the greater omentum transposition has been used
in fracture bone healing. The objective of this study, was
to investigate the efficacy of omentum transposition on the
healing of tibial bone fracture of dogs
Materials and Methods
Experimental Animals Design
Ten healthy mongrel adult dogs (2-3years old), weighing 12-
18 kg were used in this study. Dogs were housed in indi-
vidual cages, fed with commercial food and given water ad
libitum. The animals were kept in their respective cages for
15 days for acclimatization before experimentation. Broad-
spectrum antibiotic injection of 22000IU pencillin and 20mg
streptomycine oxytetracycline (Cipla, India, 200 mg), 1 ml/kg
was given IM daily for five days. Antihelmintic injection of 0.4
mg/kg Ivermectin (Biomectine, Vetoquinol Ltd. Lure cedex,
France, 10mg) at 0.4 ml/kg concentration subcutaneously
(SC) was given on the first day and day 14 of acclimatization.
The experimental protocols, animal ethics and animal wel-
fare were approved by the Animal Care and Use Committee
(VETBAG/12.2.013/Surg 7), College of Veterinary Medicine,
Baghdad University. Dogs were randomly divided into two
groups (n=5). The tibial bone of the left side in all animals
was fractured. In the first group, referred as the positive con-
trol group (CG), the tibial induced fracture was reduction and
fixation with intramedullary pin. In the second group, the
tibial induced fracture was treated with omental transposition
group (TG) All animals of both groups were euthanized on
days 56 post operations (PO).
Control Group (CG)
The tibial fracture was immediately reduced and fixation us-
ing the standard normagrade intramedullary pinning tech-
nique, which described below. Radiological assessment data
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RESEARCH PAPER
were recorded at the end of the study on day 56 PO. The
animals were then euthanized and the splinting bone was
collected for histopathology.
Anesthesia
The dogs were fasted for two hours prior to the anesthe-
sia. Induction of anesthesia was achieved by intramuscular
injection of a mixture of 15mg/kg Ketamine hydrochloride
(Bioketan, Vetoquinol Biowet, Sp. Zo.O, France), 5mg/kg
of Xylazine hydrochloride (ILIUM XYLAZIL-20, Australia) and
Acepromazine maleate 1 mg/kg (Calmivet. Vetoquinol. Ltd.
Lure cedex, France).
Modified Surgical Protocol
Hair on the skin of the dog was clipped from the lateral and
caudal aspect of the left hind limb up to the level of the wing
of the ilium dorsally to the level of the sacrum caudally and
the tarsal joint distally. The skin was disinfected with Chlo-
rohexidine gluconate (hibiscrub, 4% w/v Durham, UK), 70%
Isopropyl alcohol (Jaya Pelita Pharma. SDN. BHD) and disin-
fected with 1.8% tinctured Iodine (Jaya Pelita Pharma SDN.
BHD).
The paw was excluded from tarsal joint to the end of the limb
and from the surgical area, by placing a latex glove over the
distal extremity and securing it to the limb with a tape. The
glove was covered with sterile skin towel and secured to the
limb with towel clips. The animal was placed on the right
lateral recumbency. The left hind limb was draped with the
aperture of the fenestrated drape located at the intended
operation site. The stifles joint was palpated and tarsal joint
used as landmarks. The skin was curvilinear on the cranio-
medial crus from stifle to tarsal joint, using a scalpel blade ≠
21. Subcutaneous tissue was incised on the same line using
scalpel blade size 15, the muscle separated by blunt dissec-
tion using Mayo scissors to expose the tibial bone. A hand
saw was used to induce fracture at the distal third of tibia.
The fracture of tibial bone was immediately fixed using nor-
mograde intramedullary pinning. To insert a Steinmann pin
in the tibia, the pin is placed through the proximal fragment
entering just medial and caudal to the tibial tuberosity of the
medial side of the patellar ligament. Following introduction
of the pin in the proximal fragment, the fracture is reduced
and the pin is seated normally (Fig. 1).
A simple continuous suture was applied on the superficial
fascia using 3-0 Vicryl (Biovek, Dynek Pty Ltd, Australia) with
simple continuous suture and the skin was closed with using
a 3-0 Vicryl subcuticular suture pattern. All animals were giv-
en postoperative analgesia of 10 mg/kg Tramadol hydrochlo-
ride (Domadol® India, 50 mg) at 0.2 ml/kg intramuscular by
administered at 12-hour intervals for three consecutive days.
Coaptation Meson Meta splint is applied to the planter side
of the limb over padding and then taped into place for one
week as supporting external splint.
Omental Pedicle Transposition (TG)
Hair on the midline abdominal wall was clipped off and dis-
infected from the xiphoid cartilage to the pubic region. Fol-
lowing splinting of tibial fracture bone as described in the
control group, the position of the animal was changed to
dorsal recumbency to create the omental pedicle. The ab-
dominal wall was incised at the ventral midline 5-cm from
xiphoid cartilage to umbilical region with scalpel blade size
20. Subcutaneous tissue and fascia was incised using scalpel
blade size 15. The omentum was extended by releasing the
dorsal leaf of omentum by blunt dissection from the duode-
num and descending colon, which was then incised inversion
L-shaped to provide double length of the omental pedicle
(Fig. 2).
The omental pedicle was extended caudally on the peritone-
al surfaces of the abdominal wall, at the level of the femoral
bone. A separation between the semimembranous and ad-
ductor muscles was created by blunt dissection using curved
Kelly forceps. The upper part of the abdominal wall was
then perforated and the omental pedicle gently retracted
using curved Kelly forceps. The animal’s position was then
changed to the right lateral position. Grasping the omental
pedicle with curved Kelly forceps, the former was draw to the
site of fracture bone through the tunnel under the skin. The
omentum was wrapped around the fracture bone area and
fixed with long digital extensor muscle by two stitches of 3.0
vicryl simple interrupted suturing (Fig. 3).
The midline incision was closed using 3.0 vicryl simple con-
tinuous sutures and subcutaneous tissue was closed using
3.0 vicryl, modified Cushing sutures. The skin was closed
using 3.0 vicryl subcuticular sutures. Muscles and subcuta-
neous tissue of the crus were closed using 3.0 vicryl simple
continuous sutures and lastly the skin was closed using 2.0
vicryl subcuticular sutures.
Radiography
Radiographs (craniocaudal, mediolateral) of the tibia were
taken on immediate postoperative time based on ‘four A’s
(apposition, alignment and angulation and apparatus po-
sition) and then at 8 weeks (56 days PO). On follow-up ra-
diographs, apposition and alignment of fractured fragments
with adequate cortical contact between fractured fragments
were maintained at immediate postoperative day radio-
graphic evaluation of activity, clinical union was noticed at
56th postoperative day in all treated cases and secondary
bone healing was evidenced by formation of periosteal cal-
lus. Clinical union was evidenced by closure of fracture gap
and soft tissue swelling at fracture site was noticed
Histological Examination
The animals were euthanized on 56 day PO after radiographi-
cal assessment. All the soft tissues were removed around the
bones and the osteotomy site were studied grossly. A 2 cm
segment of the bone symmetrically encompassing the repair
site was harvested. The samples were fixed in phosphate-
buffered formalin, decalcified in 10% nitric acid followed by
rinsing in tap water for 5 hours and air-drying, then put in
formalin for one more week. The samples were then dehy-
drated, and embedded in paraffin wax. Five-micrometer se-
rial sections of the midsubstance of the bone were cut. The
sections were stained with hematoxylin and eosin, and exam-
ined in a blinded fashion. Histological sections were evalu-
ated for evidence of bone union and the relative amounts of
bone, cartilage, and fibrous connective tissue and periosteal
callus surrounding the osteotomy site.
Result
Lameness Grade
A lameness grade was assigned on the basis of severity of
clinical signs on operatively at 1st, 7th, 14th, 30th and 56th
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postoperative day to assess the response to treatment.
Weight bearing was graded as followed by Vasseur et al.
(1995). The lameness grade was 5 on operative day. Dogs
started to bear weight on the operated limb on 7th to 10th
postoperative day and walked normally without any signs of
pain or limping 15 to 20 days after the operation. The lame-
ness grading is represented in Table 1.
Functional Outcome
Functional outcome was evaluated on the 56th postopera-
tive day and categorized as excellent, good, fair and poor
in all animals (Clark, 1986). The assessment was subjective
and based on individual evaluation. The functional limb out-
come of the treated group was graded as excellent in three
cases (60.0%) and good in two cases (40%), rather than con-
trol group was graded as good in two (40%), fair in two (40%)
and poor in one case (20%)(Table 1).
Postoperative Complications
Seroma formation was observed in two case of control group
at 1st postoperative day. Abduction rotation of operated
limb was noticed at 7th postoperative day in one case of
treated group
Table 1: Lameness grades and Functional outcome
Radiology
Radiography of control group on day 56 post operation re-
vealed still fracture line, little periosteal callus formation at
the osteotomy site, soft tissue swelling at fracture site, inade-
quate cortical contact between fractured fragments, radiolu-
cent at the site of fracture, periosteal reaction is not appeared
and no clinical union (Fig. 4). Radiography of treated group
on day 56 PO showed complete disappeared of fracture line,
characteristic periosteal reaction, good remodulation of os-
teotomy site, radiopaque at the site of fracture, complete ra-
diographic union and clinical union was evidenced by closure
of fracture gap (Fig. 5).
Histopathology
The results of histopatholoy on day 56th PO showed the
greater omentum changed to a dense tissue attached firmly
to the periosteal bone (Fig. 6). The trabicular bone complete-
ly bridged the bone defect in treatment group, highly vascu-
lar at the periosteal site of newly trabicular bone and scanty
of endochondral site of ossification for replacement tissue
formed during the remodeling of bone matrix (Fig. 7) and
corticule bone is then laid down to reconstruct the shaft walls
of the fracture bone (Fig. 8). Whereas, in control group the
fracture line was only partially bridged by mixed soft callus
and fibrocartilaginous tissue and osteoblasts begin to form
spongy bone, which bulges from the fracture site and slowly
calcifies (Fig. 9).
Discussion
The results of this study showed that the omental pedicle
promote healing of distal third tibial bone fracture. The ra-
diological results of this study showed that the treated group
(omental transposition) complete disappeared of fracture
line with remodeling of callus formation and complete radio-
graphic union, while the control group still revealed fracture
line and few periosteal callus formation. Hispathological ex-
amination of treated group demonstrated remodeling of tra-
becular bone, good osteoblastic appositional surfaces and
active of ossification processes. This result is in agreement
with previous studies which reported that healing of tibeal
defect treated with omental graft can influence bone heal-
ing through augmentation of vasculogenesis, as an essential
element for proper bone healing (Oloumi et al., 2006). It is
to be noted that this is the first study undertaken where the
omental pedicle were used in fracture of long bone.
Normal weight bearing on all limbs at rest and when walking
which was graded as 1 and this was attributed to omentum
might secrete analgesic substances such as opioids, Beta-en-
dophrin, Met-enkephalin, neurotransmitter including gamma
aminobutyric acid (GABA), norepinephrine and other mono-
amines which play a role in the modulation of pain. Agner
et al. (2001) reported the putative role of omentum analge-
sic substance in the mechanism of modulation of pain. Dogs
started to bear weight on the operated limb on 7th to 10th
postoperative day and walked normally without any signs
of pain or limping 15 to 20 days after the operation. In the
present study, all the dogs were evaluated for functional out-
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come at 56th postoperative day, 3 cases (60%) had a success-
ful return to function in 30 days of tibial fractures treated by
omentum pedicle. The full functional limb of control group
was with an average of 49 days.
Bone fracture results in disruption of the marrow architecture
and blood vessels within and around the fracture site. During
bone repair, the three components of the normal bone blood
supply, medulary, periosteal, and osseus can be enhanced
according to physiological need (Glowacki, 1998). The role
of the vascular response in the healing of fractures has been
well documented in the literature (Kurdy et al., 1997), so that
the fracture of the tibia in the dog mostly suffering of delay
and non-union due to poor in blood supply leading to slow
healing (Leonard, 1971).
Vascular invasion of the fracture hematoma is a crucial step
in the progress to union, as Chidgey et al. (1986) demon-
strated that the return of mechanical integrity of the fractured
bone is in direct relation to the vascular reorganization at the
fracture site. The vascular response observed during fracture
healing may be conveniently divided into two phases, an ini-
tial and generalized vasodilation response for whole injured
limb (Gregg et al., 1983) and more simultaneous of localized
vascular invasion of the hematoma and fracture gap, which
characterized by new capillary and small vessel formation
(Rhinelander et al., 1962). The maximum increase in blood
flow at the fracture site has been observed during the first 14
days after injury (Taylor et al., 1991).
In this study, the callus was more prominent in the treatment
group and also the vasculogenesis was significantly higher in
treatment group. Since the only variable between the two
groups was the presence of greater omentum transposition
in treatment group, this difference can be attributed to it.
In tibial fractures, the pattern and rate of fracture healing is
ultimately dependent on the viability of the local circulation
and its capacity to elicit a response (Trueta, 1963).
The greater omentum might play important role in the heal-
ing that might be a number of polypeptide growth factors
possessed potent angiogenic properties have recently been
identified. Zhang et al. (1997) analyzed the level of vascu-
lar endothelial growth factor (VEGF) protein in a number of
rat tissues. The omentum demonstrated the highest VEGF
secretion rate as well as the highest concentration of VEGF
protein of the various rat tissues and organs examined. They
suggested that VEGF is the major angiogenic factor pro-
duced by omentum and possibly underlies the mechanism
omentum-induced angiogenesis. Also, it has been demon-
strated that VEGF activity is essential for normal angiogen-
esis and appropriate callus architecture and mineralization in
response to bone injury and the production of this growth
factor is the major mechanism by which angiogenesis and
osteogenes are tightly coupled during bone repair (Peng et
al., 2002.; Carano and Filvaroff, 2003; Vadasz et al., 2004).
In the other study by Matoba et al. (1996), omental implan-
tation was used for repair of perforated gastric ulcer in rat.
Greater anti-inflammatory, angiogenic activity and acceler-
ated collagen synthesis were seen in omental implantation
group. Basic fibroblast growth factor (bFGF)-mediated an-
giogenesis was noted in this group, as well as transforming
growth factor beta-1 (TGF-b1) activity within and around the
omentum, resulting in abundant collagen production. Both
bFGF (Liang et al., 1999) and TGF-b (Bostrom and Asnis
1998) are reported to have positive effects on bone repair.
The angiogenic activity of omental fat is also documented
(Silverman et al., 1988).
Activation of the omentum at the site of the injury created,
led to the expansion of the mass of non-adipose part (milky
spots), increased blood vessel density and as well as in-
creased macrophages, B-lymphocyte, T-lymphocyte, mast
cells, and stromal cells population which were important fac-
tor for bone regeneration. Macrophage release platelet-de-
rived growth factor (PDGF) and transforming growth factor-
beta 1, both of which stimulate bone production (Lieberman
et al., 2002).
The fracture bone within hours, a transient extraosseous
blood supply emerges from surrounding soft tissues, revas-
cularizing the hypoxic fracture site (McLaughlin, 1991). Mon-
onuclear phagocytes delivered by these new vessels assist in
the removal of necrotic bone and aid in construction of the
callus. Macrophages are also believed to orchestrate the or-
derly sequence of cutaneous wound healing and would play
a similar role in fracture repair. They contain several growth
factors, such as fibroblast growth factor (FGF), and initi-
ate fibroplasia both in soft tissue as well as in bone repair
(McLaughlin, 1991).
Low oxygen tension, poor vascularity, growth factors, and
interfragmentary strain influence the elaboration of a carti-
laginous callus. The periosteum surrounding the fracture site
thickens prior to undergoing chondrogenic transformation;
thereby producing an external callus entirely vascularized by
extraosseous vessels (Remedios, 1999). An internal or med-
ullary callus develops from the endosteal cell layer and is
confined to the medullary canal and receives its blood sup-
ply derived from medullary arterioles (Dudley et al., 1997).
The presence of a fibrocartilage layer within the medullary
canal temporarily interrupts the medullary blood flow across
the fracture gap. Both the external and the internal callus
constitute the “bridging callus” (Binnington, 1990). Although
the mechanical properties of this calcified fibrocartilaginous
tissue have not been reported, these structures contribute
greatly to the restoration of strength and stiffness within the
fracture gap, thus allowing formation of compact bone. Min-
eralization of the soft callus proceeds from the fragment ends
toward the center of the fracture site and forms a “hard cal-
lus” (Rahn, 2002).
The most extensively studied osteoinductive factors which
are released from omentum such as transforming growth
factor-b superfamily of morphogenetic proteins, comprising
structurally and functionally related proteins, such as trans-
forming growth factor-b and bone morphogenetic protein
(BMP), which play significant roles in embryonic develop-
ment and tissue repair as well as in bone development (Miya-
zono et al., 2004). Transforming growth factor-b, one of the
major growth factors present in bone matrix, is a polypep-
tide synthesized and secreted in bone cultures. It is believed
that the primary role of transforming growth factor-b in bone
formation is to increase the pool of committed osteoblasts.
BMPs are identified and cloned after the discovery that ex-
tracts from demineralized human bone matrix induce ectopic
bone formation (Wozney et al., 1988). The major angiogenic
factors include fibroblast growth factors, platelet-derived
growth factor and vascular endothelial growth factor (VEGF).
Fibroblast growth factors and VEGF stimulate endothelial cell
production of proteases and plasminogen activators that de-
grade the vessel basement membrane and allow endothelial
cell proliferation and migration (Cross and Claesson-Welsh
2001). Endothelial cells and endothelial progenitor cells
then assemble to form new blood vessels and secrete key
factors, such as platelet-derived growth factor and angiopoi-
etin-1, to recruit smooth muscle cells and pericytes to stabi-
lize and support the newly formed blood vessels (Lindahl et
al., 1998). Growth factors, which stimulate angiogenesis, also
drive bone repair and regeneration. In conclusion, it is ap-
peared the omental pedicle enhancing healing of the distal
third tibial fracture.
Acknowledgements:
Authors would like to thank Surgery Department/ College of
Veterinary Medicine/ Baghdad University which was provided
the facilities for accomplished the research.
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RESEARCH PAPER
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The omentum has been utilized in neurosurgery for over 30 years. However, the anatomical and physiological bases for its applications have not been described in great detail. In this paper, we will review the current status of the omentum applications for the management of central nervous system disorders.
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The early vascular response is essential for the normal progress of fracture healing and fracture site blood flow has been shown to reach a peak in the first two weeks after injury. Angiogenesis is an important step in this response as new vessel formation is necessary to vascularize the fracture haematoma and the fracture gap. Changes in serum levels of a low molecular weight endothelial stimulating angiogenic factor (ESAF) have been previously reported in a group of four patients with tibial fractures. In this group, ESAF levels were measured on three occasions only and at different time intervals. We present a more detailed profile of serum ESAF level changes in the first 14 days after the fracture.
Randomized, controlled trails of the efficacy of carprofen, a non-steroidal anti-inflammatory drug in the treatment of osteoarthritis in dogs Novel regulators of bone formation: molecular clones and activities
  • Pb Vasseur
  • Al Johnson
  • Sc Buderberg
  • Jb Linwln
  • Jp Toombs
  • Jg Whitebain
  • El Lentz
Exp. Mol. Pathol., 77: 145–148. | Vasseur, PB, Johnson AL, Buderberg SC, Linwln JB, Toombs JP, Whitebain JG and Lentz, EL (1995). Randomized, controlled trails of the efficacy of carprofen, a non-steroidal anti-inflammatory drug in the treatment of osteoarthritis in dogs. J Am Vet Med Assoc, 206: 807-811. | Wozney, JM, Rosen, V, Celeste, AJ, Mitsock, LM, Whitters, MJ, Kriz RW, Hewick, RM and Wang, EA (1988). Novel regulators of bone formation: molecular clones and activities. Science., 242: