Download Use of bovine pericardium (Tutopatch®) graft for surgical repair of

Veterinary Ophthalmology (2014) 17, 2, 91–99
DOI:10.1111/vop.12047
Use of bovine pericardium (Tutopatchâ) graft for surgical repair of
deep melting corneal ulcers in dogs and corneal sequestra in cats
Thomas Dulaurent,* Thierry Azoulay,† Frederic Goulle,‡ Alice Dulaurent,* Marielle Mentek,§
Robert L. Peiffer¶ and Pierre-Francßois Isard*
*Centre Hospitalier Veterinaire, 275 Route Imperiale, Saint-Martin Bellevue 74370, France; †Clinique Veterinaire, 28 rue du Faubourg de Saverne, Strasbourg 67000, France; ‡Clinique Veterinaire, Parc d’activite Mermoz, 19 Avenue de la for^et, Eysines 33320, France; §Laboratoire HP2, INSERM, U1042,
Universite J. Fourier, Grenoble 38706, France; and ¶Bucks County Animal Ophthalmology, 4895 Gloucester Dr, Doylestown, PA, 18902, USA
Address communication to:
T. Dulaurent
Tel.: +33 (0)4 50 60 09 00
Fax: +33 (0)4 50 60 14 86
e-mail: ophtalmologie@chvsm.
com
Abstract
Objective To evaluate the efficacy of bovine pericardium (BP) graft in the treatment of
deep melting corneal ulcers in three dogs and corneal sequestra in three cats.
Procedure Three dogs with keratomalacia affecting the deep third of the stroma and
three cats with corneal sequestrum were evaluated and underwent surgery. Following
keratectomy, BP material was placed into the keratectomy bed and sutured to the recipient cornea with 9/0 polyglactin suture material. Postoperative treatment with topical
and systemic antibiotics, systemic nonsteroidal anti-inflammatory agents, and topical
atropine was prescribed. Follow-up examinations were carried out 1, 2 weeks, 1 and
2 months after the surgery and consisted of a complete ophthalmic examination. Optical coherence tomography (OCT) was performed 1 and 2 months after the surgery in
one dog and in one cat.
Results At 1 week, corneal neovascularization was present around the BP graft in all
cases. Four weeks after the BP graft, in two dogs and in all cats, the vascularization was
regressing and the graft was integrated into the cornea, which was regaining transparency. Topical treatment with anti-inflammatory agents was then prescribed for
2 weeks. Two months after the surgery, 5 of 6 corneas in two dogs and three cats had
healed with focal corneal scarring. The remaining dog had progression of the keratomalacia involving the deep BP graft that required additional surgery, but became blind.
Conclusion Bovine pericardium graft offers a promising option for surgical reconstruction of the cornea following keratectomy for the management of corneal ulcers and
sequestra.
Key Words: cat, cornea, dog, pericardium, sequestrum, ulcer
INTRODUCTION
Corneal ulcers are frequently traumatic in origin. Secondary bacterial infection is common. The normal corneal
healing process requires the production of proteases and
collagenases. They aim at removing devitalized cells and
debris from the cornea. Corneal epithelial cells, fibroblasts, and some bacteria and fungi produce these proteolytic enzymes, which may have detrimental effects on the
corneal stroma. The progressive dissolution of the corneal
stroma eventually leads to keratomalacia. These ‘melting’
ulcers may be unresponsive to aggressive medial therapy
and require specific surgical procedures.1
Corneal sequestrum is a common disorder in cats,2 particularly in the Persian and Himalayan breeds. It is rarely
© 2013 American College of Veterinary Ophthalmologists
seen in dogs3 and in horses.4 In cats, it has been associated
with feline herpes virus 1 (FHV-1) or chronic corneal irritation by physical factors such as entropion or distichiasis.2,5–8 This condition appears as a brown to black lesion
of corneal necrosis of 1–2 mm in diameter to more than
half of the cornea in size. It may be associated with
intense corneal neovascularization. Ocular pain ranges
from none to marked.2 Debridement of necrotic corneal
tissue by keratectomy facilitates resolution.2,6,9–11 If the
keratectomy is deep, a graft may be necessary.2
The goal of treatment of corneal disease is to restore
structural integrity with minimal alteration in corneal
transparency. Many surgical techniques have been
described for the management of keratomalacia and
sequestrum: keratectomy combined with conjunctival
92 dulaurent
ET AL.
grafts,5,12–16 corneo-conjunctival transposition,9,17 porcine
small intestinal submucosa graft,18–23 amniotic membrane
transplantation,24–28 and heterologous penetrating keratoplasty.29,30
Over the past decades, there has been a growing interest
in the use of bovine pericardial patch in the surgical management of many pathologic conditions in humans31
including carotid dissection,32 cardiac defects,33–35 or tracheal rupture.36 In human ophthalmology, several studies
have reported the use of BP in the management of corneal
wounds37,38 or as a wrapping material for hydroxyapatite
orbital implants.39,40 In veterinary ophthalmology, Barros
et al.41–43 described the use of equine pericardium as a keratoprosthesis in the dog. In their reports, equine pericardium was successfully used for the surgical treatment of
experimentally created superficial keratectomy and of corneo-scleral reconstruction after a traumatic perforation or
the removal of an epibulbar melanoma in two dogs.
The purpose of the present study was to evaluate the
use of BP for the repair of keratomalacic corneal ulcers in
dogs and corneal sequestra in cats.
MATERIAL AND METHODS
Three dogs with keratomalacia affecting the deep third of
the cornea and three cats with corneal sequestra were
included in this study. All animals were adults between 2
and 9 years of age for dogs and 4 and 8 years for cats.
Each animal underwent a complete ophthalmic examination: Schirmer tear test, slit-lamp biomicroscopy, and
intraocular pressure measurement by rebound tonometry.
A Seidel test was performed in the dogs.
In all three dogs, the melting corneal ulcer was present
paracentrally, without corneal vascularization. It affected
the deep third of the cornea (Fig. 1). The Seidel test was
negative in all animals. Physical examination was normal.
The owners of Dogs 1 and 2 reported ocular trauma
3 days before referral. All dogs had been treated with
topical and/or systemic antibiotics and topical acetyl
Figure 1. Dog 1: melting corneal ulcer located at the axial cornea.
cysteine. The clinical data of each animal are presented in
Table 1.
In all three cats, the sequestrum was central and associated with peripheral neovascularization (Fig. 2). By history, the sequestrum was accompanied by a 3-month
history of ocular disease in Cat 1 and several weeks in
Cats 2 and 3. The sequestrum was well tolerated in Cat 1
and associated with a moderate level of pain in Cats 2 and
3. Physical examination was normal in all three cats. Polymerase chain reaction testing for FHV-1 was performed
in all cats, and the result was positive only for Cat 1.
Treatment prior to surgery included topical and/or
systemic antibiotics, topical acetyl cysteine, and/or topical
antiviral agents.
Surgical procedure
General anesthesia was induced by intravenous injection
of medetomidine (Domitorâ; Janssen, Issy-les-Moulineaux,
France) 2 lg/kg, and ketamine (Ketamine Virbacâ; Virbac, Carros, France) 5 mg/kg, followed by isoflurane gas
(Isoflurane Belamontâ;Nicholas Piramal, London, UK)
inhalation. The affected eyes were routinely prepared for
ocular surgery with 5% povidone iodine solution
antisepsis.
In the dogs, keratectomy to remove necrotic and collagenolytic tissue was performed using curved, blunt-tip
Castroviejo scissors. In all dogs, the surgically removed
cornea was submitted for bacterial culture.
In the cats, a corneal trephine was used to demarcate
unhealthy cornea around the lesion, which was excised
with sharp dissection.
The 40 9 50 9 0.1 mm plaque of sterile BP (Tutopatchâ; Tutogen, Metz, France) was removed from its
package and trimmed with a corneal trephine to obtain a
circular graft of the same diameter as the keratectomy
defect. According to the manufacturer’s recommendations,
the smooth side was marked with a corneal marking pen
prior to rehydration in a solution of gentamicin 4 mg/mL
(G4â; Virbac) for 1 min. The graft was then placed over
the keratectomy bed, the rough side in contact with the
stroma. Then, it was fixed to the healthy cornea with a
simple interrupted, simple continuous, or Ford interlocking continuous suture pattern of 9/0 polyglactin 910
(Vicryl monofil absorbable suture; Ethicon, Janssen,
Noisy-le-grand, France) (Figs 3 and 4). An Elizabethan
collar was recommended for 1 week postoperatively.
Postoperative treatment consisted of topical administration of tobramycin eye drops (Tobrex; Alcon, RueilMalmaison, France) three times daily for 4 weeks and
atropine 1% eye drops (Atropine Faure 1%, Paris, France)
three times the day after surgery and then once daily for
three additional days. Each animal received oral amoxicillin and clavulanic acid (Synuloxâ; Pfizer, Paris, France)
12.5 mg/kg twice daily for 10 days and oral tolfenamic
acid (Tolfedineâ; Vetoquinol, Lure, France) 4 mg/kg once
daily for 1 week.
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 17, 91–99
pericardium graft for repair of corneal defect 93
Table 1. Clinical data and outcome of dogs with melting corneal ulcers and cats with corneal sequestra treated with bovine pericardium (BP)
grafts
Dogs
Cats
Case
Breed
Age/gender
Affected eye
Bacteriology
Complication
Outcome
1
7-year-old male
OS
Pseudomonas aeruginosa
None
Visual
2
German short-haired
pointer
Japanese Spaniel
2-year-old female
OD
Pseudomonas aeruginosa
Not visual
3
1
2
3
Britain Spaniel
DSH
DSH
Persian
9-year-old
4-year-old
8-year-old
7-year-old
OS
OS
OS
OD
No growth
Not Performed
Not Performed
Not Performed
Extension of the
keratomalacia
None
None
None
None
male
neutered female
neutered female
neutered male
Visual
Visual
Visual
Visual
Figure 4. Cat 3: intraoperative photograph of Cat 3 following
suturing of the bovine pericardium (BP) graft into the keratectomy
bed.
Figure 2. Cat 3: corneal sequestrum and keratitis.
RESULTS
Figure 3. Dog 2: intraoperative photograph of Dog 2 following
suturing of the bovine pericardium (BP) graft into the keratectomy
bed.
Follow-up examinations were performed 1, 2, 4, and
8 weeks following surgery and consisted of slit-lamp
biomicroscopy, IOP measurement, and indirect ophthalmoscopy. OCT (Opkoâ; EDC-Lamy, Carvin, France) was
performed 4 and 8 weeks after the surgery in Dog 1 and
Cat 3 to assess the BP graft interface and assimilation by
the cornea.
Bacterial culture revealed infection with Pseudomonas aeruginosa in Dog 1 and Dog 2, sensitive to the antibiotics
prescribed. No bacteria were isolated from the sample
from Dog 3.
The follow-up examination performed at 1 week
revealed prominent superficial and deep peripheral corneal
neovascularization extending to the margins of the graft.
Fluorescein staining was positive overlying the graft. Dog
2 presented with a painful eye; keratomalacia had extended
to the previously uninvolved cornea as well as the BP
graft, eventually leading to corneal perforation (Fig. 5).
This animal underwent a successful bridge conjunctival
graft after removal of the infected BP graft. Cat 3 developed moderate blepharospasm and serous ocular discharge
with noticeable discomfort postoperatively; the other
patients did not show signs of ocular discomfort.
At 2 weeks, corneal vascularization was still present, but
the fluorescein staining was negative with the exception of
Cat 3 that demonstrated a small epithelial defect over the
graft. Ocular discomfort had resolved in all animals.
At 4 weeks, the corneal vascularization was regressing.
The BP graft was opalescent in all patients (Figs 6 and 7)
except for Dog 2 that had undergone the conjunctival
graft placement and Cat 3 in which the BP graft remained
opaque. Suture material was removed when still present.
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 17, 91–99
94 dulaurent
ET AL.
Figure 5. Dog 2: aspect of the eye 1 week postsurgery. Progression
of the keratomalacia involving the graft.
cornea appeared as a lamellar structure, whereas the BP
graft appeared as a homogeneous, nonlamellar structure
on which the epithelium migrated.
When the epithelial barrier was restored (as evidenced
by slit-lamp examination and negative fluorescein staining), topical dexamethasone phosphate (Sterdexâ; Thea,
Clermont-Ferrand, France) was prescribed for each dog
and topical indomethacin (Indocollyreâ; Chauvin, Montpellier, France) for each cat, twice daily over 2 weeks so as
to minimize residual corneal vessels.
Two months after the surgery, the corneas of Dog 1
and Dog 3 were translucent, and only a focal central scar
was visible; the scar was less visible in retroillumination
(Fig. 10) than in transillumination (Fig. 11). A paracentral
corneal scar was present in the three cats, and residual
corneal vascularization was more prominent than in the
dogs, despite the medical treatment (Fig. 12). OCT was
performed on Dog 1 (Fig. 13) and Cat 3 (Fig 14). The
epithelium appeared normal, and the cornea was no longer
deformed in Cat 3. However, the corneal stroma was
much thinner in the graft region in Cat 3. The transition
between the graft and the stroma also remained visible
with OCT.
No recurrence of the corneal sequestrum was observed
in the cats up to 6 months postoperatively. All patients
demonstrated vision in the affected eye, except Dog 2
where corneal opacification persisted following removal of
the conjunctival graft.
DISCUSSION
Figure 6. Dog 1: aspect of the eye 1 month postsurgery. Corneal
neovascularization and fibrosis.
Figure 7. Cat 3: aspect of the eye 1 month postsurgery. Corneal
neovascularization, inflammatory cellular infiltration, and corneal
edema.
OCT was performed on Dog 1 and Cat 3; epithelial healing was complete in both Dog 1 (Fig. 8) and Cat 3. The
general shape of the cornea was normal in Dog 1, but Cat
3 demonstrated stromal ectasia and associated corneal
deformation (Fig. 9). The transition between the graft and
the recipient stroma was clearly visible; the underlying
Over the past decades, there has been growing interest in
regenerative medicine, which aimed at repairing, replacing, and regenerating damaged tissues.44,45 BP grafts have
been extensively used in human patients in different pathologic conditions31 including arterial32 or venous46 dissection, tracheal rupture,36 cardiac defects such as tetralogy
of Fallot35 or atrial34 or ventricular33 septal defect, diaphragmatic resection,47 and abdominal wall defects.48 In
the field of ophthalmology, BP patch transplantation has
been described for the management of neurotrophic
corneal ulcers,49 corneal perforation,37,38 corneo-scleral
reconstruction after tumor resection,50 orbital floor reconstruction,51,52 and to cover glaucoma drainage devices53,54
or hydroxyapatite orbital implants.39,40
In veterinary ophthalmology, various surgical techniques
have been described for the management of deep melting
corneal ulcers or corneal sequestra including conjunctival
grafts,5,12–16 corneo-conjunctival graft,9,17 lamellar keratoplasty,11 penetrating keratoplasty,29,30 amniotic membrane transplantation,24–28 equine renal capsule graft,55
porcine SIS graft.18–23 While these techniques are
associated with a high success rate, degree of restoration
of corneal transparency and thus quality of vision is variable.6,9–30 Optimal reconstruction would maintain a clear
visual axis to preserve vision.
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 17, 91–99
pericardium graft for repair of corneal defect 95
Figure 8. Dog 1: Optical coherence tomography
(OCT) aspect of the cornea 1 month postsurgery.
The epithelial barrier is intact. The global shape
of the cornea is normal.
Figure 9. Cat 3: Optical coherence tomography
(OCT) aspect of the cornea 1 month postsurgery.
The epithelium covers the graft. A corneal facet is
present and affects the shape of the cornea. An
important corneal edema is also visible.
Figure 10. Dog 1: retroillumination aspect of the eye 2 months
postsurgery. The scar is translucent.
Figure 11. Dog 1: same picture in transillumination. The scar is
more visible.
The use of SIS graft has been described by Vanore
et al.22 in seven eyes (two cats and five dogs) presenting
with deep melting corneal ulcers. No severe complications occurred, and vision was preserved in all the cases.
Featherstone et al.20 described the use of SIS in 10 cases
of feline corneal disease (four cases of deep stromal
ulcers, one case of melting ulcerative keratitis, and five
cases of corneal sequestra). One case of deep stromal
ulcer required a complementary conjunctival graft
because of early positive Seidel test. The melting ulcera-
tive keratitis required enucleation secondary to extensive
keratomalacia. The five cases of corneal sequestra were
successfully treated by SIS graft. In a recent retrospective
study of one hundred and six eyes treated with SIS
graft,23 Goulle showed that vision was preserved in all
eyes at 3 months postsurgery; in 69.8% of the cases, the
cornea was either transparent or scarring minimal and
focal, while in 30.2% of the cases, a more extensive scar
was observed. Minor complications occurred in 8.5% of
the cases, including partial integration of the SIS, and in
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 17, 91–99
96 dulaurent
ET AL.
Figure 12. Cat 3: retroillumination aspect of the eye 2 months
postsurgery.
22.6% faint or mild corneal pigmentation, without
impairment of vision. In cases followed over a period
longer than 3 months, progression of pigmentation
impaired vision in five dogs.
Amniotic membrane transplantation has been described
by Barachetti et al.6 for the treatment of feline corneal
sequestra. In their study, corneal transparency was
restored in five of seven treated eyes, with no recurrence
of the disease 9 months after the surgery. Barros et al.25
reported the successful use of amniotic membrane in the
management of severe bullous keratomalacia in a
Yorkshire dog. Amniotic membrane transplantation has
also been used in the management of a large corneal epithelial cyst in a dog,56 in the reconstruction of the cornea
after the excision of dermoids57 and ocular tumors in dogs
or ankyloblepharon in cats,25 and for ocular surface reconstruction in horses.26
A review of reported success rates of different procedures in cases of deep melting corneal ulcers and corneal
sequestra is summarized in Table 2.
Barros et al.43 have described the use of equine pericardium in the surgical treatment of experimentally created
superficial keratectomy in twelve dogs. The study included
a histologic analysis of the grafted cornea, at days 7, 15,
30, and 100 after implantation. The equine pericardial
graft was well tolerated in all cases, despite a mild blepharospasm until day 15, and a chemosis for 1 week in all
animals. An inflammatory cellular infiltrate was seen histologically during all the experiment. At day 100, histologic
examination revealed fibrosis and mild inflammatory infiltrate. The epithelialization began at day 7 and was complete at day 30. The same team42 used equine pericardium
in the surgical management of a corneal perforation and
of a corneo-scleral reconstruction after the removal of a
limbal melanoma in two dogs. The equine pericardium
Figure 13. Dog 1: Optical coherence
tomography (OCT) aspect of the cornea
2 months postsurgery. The epithelium is normal,
and the interface between endogenous and
exogenous collagen remains visible.
Figure 14. Cat 3: Optical coherence tomography
(OCT) aspect of the cornea 2 months
postsurgery. The epithelium is normal, but the
stroma is thinner in the region of the bovine
pericardium (BP) graft. The interface between
endogenous and exogenous collagen remains
visible.
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 17, 91–99
pericardium graft for repair of corneal defect 97
Table 2. Literature review of the results obtained with different surgical techniques for the treatment of melting corneal ulcers and corneal
sequestra in dogs and in cats
Deep melting ulcers
Number of cases
Corneo-conjunctival
transposition
Small intestinal
submucosa graft
Corneal sequestra
Succes
rate (%)
Reference
42 dogs
88
Goulle23
7 Cats
5 dogs
2 cats
100
100
100
Vanore22
Number of cases
Success rate
Reference
17
100% with no
reccurence
100% with 4
reccurences
Andrew et al.9
34
5
6
Conjunctival graft
Amniotic membrane
transposition
24
1 dog (360° conjunctival
graft)
10 dogs (pedicle grafts
and bridge grafts)
14 dogs (pedicle graft)
1 dog
3 horses
100
Pumphrey et al.16
100
Kuhns13
100
100
100
Hakanson et al.15
Barros et al.25
Lassaline26
7
Lamellar keratoplasty
Keratectomy alone
was well tolerated and allowed an accurate healing of
affected tissues.
In our study, the patches were provided by Tutogen.
Tutopatchâ is a xenograft stem from bovine pericardium.
It is composed of collagen and elastin only. The patches
are viro-inactivated and sterilized meaning they are
cleaned of cells, bacteria, virus, DNA, and fungus.48 The
rough side of the patch should be in contact with the corneal stroma to facilitate host cell migration and neovascularization. As for the SIS and amnion grafts, there is a
specific orientation recommended by the manufacturer.
The rough side of the Tutopatch promotes integration of
the mesh and remodeling by the endogenous reparative
tissue of the patient. The smooth side of the Tutopatch
does not promote such adhesions.
The results of our clinical study are similar to those
obtained with SIS graft or amniotic membrane transplantation. A successful outcome was obtained with BP graft
in five of six eyes. In the solitary failure, we suspect that
the BP had become infected by the organism responsible
for the keratomalacia. Furthermore, the frequency of topical instillations of antibiotics on the infected corneas we
implemented may have been insufficient for the medical
management of the infection.
The biocompatibility of SIS with the cornea has been
studied in rabbits.58 Greca et al.46 have compared the bio-
6 (allograft and
heterograft)
1
44
Goulle23
100%
100% with 1
reccurence
100% with 4
reccurences
Featherstone et al.20
Featherstone and Sansom5
71% with no
reccurence
100% with no
reccurence
0%
100% with 1
reccurence
Barachetti6
Featherstone and Sansom5
Pena Jimenezet al.11
Townsend et al.10
Featherstone and Sansom5
compatibility of SIS and BP used as grafts in the inferior
cava veins of dogs; both biomaterials seem to behave similarly during the healing process. Barros et al.43 have studied the biocompatibility of equine pericardium with dogs
cornea. Our results show that the healing phases of the
cornea after BP graft were clinically similar to the SIS
graft and equine pericardium graft, initially associated
with marked vascularization of the peripheral cornea. This
phase lasted between 1 and 2 weeks. The second phase
was assimilation of the graft and re-epithelialization of the
graft surface. The third phase of vascular regression and
stromal remodeling toward transparency started approximately 3–4 weeks after the surgery. In the cats treated for
corneal sequestra, corneal neovascularization persisted
compared with dogs treated for deep melting corneal
ulcers.
Anterior segment OCT imaging is widely used in
human ophthalmology to evaluate, refine, and manage
corneal transplantation patients. It allows a precise assessment of the interaction between the graft (whatever its
type) and the recipient cornea.59–62 In our study, OCT
examination demonstrated that the graft was assimilated
by the cornea. Four weeks after the surgery, the epithelium was continuous over the graft. The interface
between the exogenous and the endogenous collagen
remained obvious 2 months after the surgery. Healing
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 17, 91–99
98 dulaurent
ET AL.
occurred without alteration in the global shape of the
cornea both in the dog and in the cat. However, the stromal thickness was reduced in the region of the graft in
the cat. While recurrence of sequestra was not observed,
the duration of follow-up precludes definitive conclusions
in this regard.
Secondary calcification has been described as a longterm complication after BP grafts in the human literature,31 and a longer follow-up period is required to assess
this potential complication in our patients.
The small number of cases included in our study does
not allow us to make any definitive conclusion, but keratectomy associated with BP graft has provided effective
treatment for corneal sequestra with resultant visual eyes.
Further investigations are required to assess more accurately the efficacy of BP graft for the treatment of infected
corneal ulcers.
REFERENCES
1. Gilger BC. Diseases and surgery of the canine cornea and sclera.
In: Veterinary Ophthalmology, Vol. II, 4th edn. (ed. Gelatt KN)
Blackwell Publishing, Ames, 2007, 690–752.
2. Stiles J, Townsend WM. Feline ophthalmology. In: Veterinary
Ophthalmology, Vol. II, 4th edn. (ed. Gelatt KN) Blackwell
Publishing, Ames, 2007, 1095–1164.
3. Bouhanna L, Lisco€et LB, Raymond-Letron I. Corneal stromal
sequestration in a dog. Veterinary Ophthalmology 2008; 11: 211–
214.
4. McLellan GL, Archer FJ. Corneal stromal sequestration and
keratoconjunctivitis sicca in a horse. Veterinary Ophthalmology
2000; 3: 207–212.
5. Featherstone HJ, Sansom J. Feline corneal sequestra: a review of
64 cases (80 eyes) from 1993 to 2000. Veterinary Ophthalmology
2004; 7: 213–227.
6. Barachetti L, Giudice C, Mortellaro CM. Amniotic membrane
transplantation for the treatment of feline corneal sequestrum:
pilot study. Veterinary Ophthalmology 2010; 13: 326–330.
7. Andrew SE. Ocular manifestations of feline herpesvirus. Journal
of Feline Medicine and Surgery 2001; 3: 9–16.
8. Williams DL, Kim JY. Feline entropion: a case series of 50
affected animals (2003–2008). Veterinary Ophthalmology 2009; 12:
221–226.
9. Andrew SE, Tou S, Brooks DE. Corneoconjunctival
transposition for the treatment of feline corneal sequestra: a
retrospective study of 17 cases (1990–1998). Veterinary
Ophthalmology 2001; 4: 107–111.
10. Townsend WM, Rankin AJ, Stiles J et al. Heterologous
penetrating keratoplasty for the treatment of a corneal
sequestrum in a cat. Veterinary Ophthalmology 2008; 11: 273–278.
11. Pena Gimenez MT, Farina IM. Lamellar keratoplasty for the
treatment of feline corneal sequestrum. Veterinary Ophthalmology
1998; 1: 163–166.
12. Peiffer R, Gelatt K, Gwin R. Tarsoconjunctival pedicle grafts for
deep ulceration in the dog and cat. Journal of American Animal
Hospital Association 1977; 13: 387–391.
13. Kuhns EL. Conjunctival patch grafts for the treatment of corneal
lesions in dogs. Modern Veterinary Practice 1979; 60: 301–305.
14. Hakanson NE, Merideth RE. Conjunctival pedicle grafting in
the treatment of corneal ulcers in the dog and cat. Journal of the
American Animal Hospital Association 1987; 23: 641–648.
15. Hakanson NE, Lorimer D, Merideth RE. Further comments on
conjunctival pedicle grafting in the treatment of corneal ulcers in
the dog and cat. Journal of the American Animal Hospital
Association 1987; 24: 602–605.
16. Pumphrey SA, Pizzirani S, Pirie CG. 360-degree conjunctival
grafting for management of diffuse keratomalacia in a dog.
Veterinary Ophthalmology 2011; 14: 209–213.
17. Parshall C. Lamellar corneo-scleral transposition. Journal of
American Animal Hospital Association 1973; 9: 270–277.
18. Lewin GA. Repair of full thickness corneoscleral defect in a
German Shepherd dog using porcine small intestinal submucosa.
Journal of Small Animal Practice 1999; 40: 340–342.
19. Featherstone HJ, Sansom J. Intestinal submucosa repair in two
cases of feline ulcerative keratitis. Veterinary Record 2000; 146:
136–138.
20. Featherstone HJ, Sansom J, Heinrich CL. The use of porcine
small intestinal submucosa in ten cases of feline corneal disease.
Veterinary Ophthalmology 2001; 4: 147–153.
21. Bussieres M, Krohne SG, Stiles J et al. The use of porcine small
intestinal submucosa for the repair of full-thickness corneal
defects in dogs, cats and horses. Veterinary Ophthalmology 2004; 7:
352–359.
22. Vanore M, Chahory S, Payen G et al. Surgical repair of deep
melting ulcers with porcine small intestinal submucosa (SIS) graft
in dogs and cats. Veterinary Ophthalmology 2007; 10: 93–99.
23. Goulle F. Use of porcine small intestinal submucosa for corneal
reconstruction in dogs and cats: 106 cases. Journal of Small
Animal Practice 2012; 53: 34–43.
24. Barros PS, Garcia JA, Laus JL et al. The use of xenologous
amniotic membrane to repair canine corneal perforation created
by penetrating keratectomy. Veterinary Ophthalmology 1998; 1:
119–123.
25. Barros PS, Safatle AM, Godoy CA et al. Amniotic membrane
transplantation for the reconstruction of the ocular surface in
three cases. Veterinary Ophthalmology 2005; 8: 189–192.
26. Lassaline ME, Brooks DE, Ollivier FJ et al. Equine amniotic
membrane transplantation for corneal ulceration and
keratomalacia in three horses. Veterinary Ophthalmology 2005; 8:
311–317.
27. Ollivier FJ, Kallberg ME, Plummer CE et al. Amniotic
membrane transplantation for corneal surface reconstruction after
excision of corneolimbal squamous cell carcinomas in nine
horses. Veterinary Ophthalmology 2006; 9: 404–413.
28. Plummer CE. The use of amniotic membrane transplantation for
ocular surface reconstruction: a review and series of 58 equine
clinical cases (2002-2008). Veterinary Ophthalmology 2009; 12
(Suppl. 1): 17–24.
29. Hacker DV. Frozen corneal grafts in dogs and cats: a report on
19 cases. Journal of American Animal Hospital Association 1991; 27:
387–398.
30. Hansen PA, Guandalini A. A retrospective study of 30 cases of
frozen lamellar corneal grafts in dogs and cats. Veterinary
Ophthalmology 1999; 2: 233–241.
31. Li X, Guo Y, Ziegler KR et al. Current usage and future
directions for the bovine pericardial patch. Annals of Vascular
Surgery 2011; 25: 561–568.
32. Kim JH, Cho YP, Kwon TW et al. Ten-year comparative
analysis of bovine pericardium and autogenous vein for patch
angioplasty in patients undergoing carotid endarterectomy.
Annals of Vascular Surgery 2012; 26: 353–358.
33. Imagawa H, Takano S, Shiozaki T et al. Two-patch technique
for postinfarction inferoposterior ventricular septal defect. Annals
of Thoracic Surgery 2009; 88: 692–694.
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 17, 91–99
pericardium graft for repair of corneal defect 99
~ez-Salgado JA, Olmos-Z
~iga JR, Perez-L
34. Santiban
un
opez M et al.
Lyophilized glutaraldehyde-preserved bovine pericardium for
experimental atrial septal defect closure. European Cells and
Material 2010; 19: 158–165.
35. Mather C, Treuting P. Onchocerca armillata contamination of a
bovine pericardial xenograft in a human patient with repaired
tetralogy of Fallot. Cardiovascular Pathology 2012; 21: 35–38.
36. Carter JJ, Evans D, Shah P et al. Iatrogenic tracheal rupture:
bovine pericardial patch repair without flap reinforcement.
Interactive Cardiovascular and Thoracic Surgery 2012; 14: 502–503.
37. Koay AC, Yew YH, Ngo CT et al. The use of preserved bovine
pericardium for emergency temporizing graft in corneal
perforation. Medical Journal of Malaysia 2008; 63: 421–422.
38. Khanna RK, Mokhtar E. Bovine pericardium in treating large
corneal perforation secondary to alkali injury: a case report.
Indian Journal of Ophthalmology 2008; 56: 429–430.
39. Gupta M, Puri P, Rennie IG. Use of bovine pericardium as a
wrapping material for hydroxyapatite orbital implants. British
Journal of Ophthalmology 2002; 86: 288–289.
40. Gupta M, Lyon F, Singh AD et al. Bovine pericardium
(Tutopatch) wrap for hydroxyapatite implants. Eye 2007; 21:
476–479.
41. Barros PS, Safatle AM, Rigueiro M. Xenologous pericardium as
keratoprosthesis in the dog. An experimental study. Proceedings,
24th Annual Meeting of the American College of Veterinary
Ophthalmologists 1993, 23.
42. Barros PS, Safatle AM, Malerba TA et al. The surgical repair of
the cornea of the dog using pericardium as a Keratoprosthesis.
Brazilian Journal of Veterinary Research and Animal Science 1995;
32: 251–255.
43. Barros PS, Safatle AM, Rigueiro M. Experimental lamellar
corneal graft in dogs using preserved equine pericardium.
Brazilian Journal of Veterinary Research and Animal Science 1999;
36: 304–307.
44. Theoret C. Tissue engineering in wound repair: the three “R”s –
Repair, Replace, Regenerate. Veterinary Surgery 2009; 38: 905–913.
45. Orlando G, Wood KJ, De Coppi P et al. Regenerative medicine as
applied to general surgery. Annals of Surgery 2012; 255: 867–880.
46. Greca FH, Noronha L, Costa FD et al. Comparative study of
the biocompatibility of the porcine small intestinal submucosa
and bovine pericardium used as grafts in the inferior cava vein of
dogs. Acta Cir
urgica Brasileira 2005; 20: 317–322.
47. Zardo P, Zhang R, Wiegmann B et al. Biological materials for
diaphragmatic repair: initial experiences with the PeriGuard
Repair Patchâ. Journal of Thoracic and Cardiovascular Surgery
2011; 59: 40–44.
48. Lai PH, Chang Y, Liang HC et al. Peritoneal regeneration
induced by an acellular bovine pericardial patch in the repair of
49.
50.
51.
52.
53.
54.
55.
56.
57.
58.
59.
60.
61.
62.
abdominal wall defects. Journal of Surgical Research 2005; 127:
85–92.
Ortuno-Prados VJ, Alio JL. Treatment of a neurotrophic corneal
ulcer with solid platelet-rich plasma and Tutopatchâ. Archivos de
la Sociedad Espanola de Oftalmologia 2011; 86: 121–123.
Scupola A, Blasi MA, Petroni S et al. Bovine pericardium for
scleral closure in transscleral local resection of choroidal
melanoma. Retina 2008; 28: 1530–1532.
Rinna C, Ungari C, Saltarel A et al. Orbital floor restoration.
Journal of Craniofacial Surgery 2005; 16: 968–972.
Schm€al F, Basel T, Grenzebach UH et al. Preseptal
transconjunctival approach for orbital floor fracture repair:
ophthalmologic results in 209 patients. Acta Oto-Laryngologica
2006; 126: 381–389.
Yalvac IS, Duman S, Izgi B. Double-layer pericardium sandwich
technique of Ahmed glaucoma valve implantation in patient with
anterior necrotizing scleritis. Techniques in Ophthalmology 2005; 3:
86–89.
Yoo C, Kwon SW, Kim YY. Pericardium plug in the repair of
the corneoscleral fistula after Ahmed Glaucoma Valve
explantation. Korean Journal of Ophthalmology 2008; 22: 268–271.
Antrade AL, Laus JL, Figueiredo F et al. The use of preserved
equine renal capsule to repair lamellar corneal lesions in normal
dogs. Veterinary Ophthalmology 1999; 2: 79–82.
Choi US, Labelle P, Kim S et al. Successful treatment of an
unusually large corneal epithelial inclusion cyst using equine
amniotic membrane in a dog. Veterinary Ophthalmology 2010; 13:
122–125.
Kalpravidh M, Tuntivanich P, Vongsakul S et al. Canine
amniotic membrane transplantation for corneal reconstruction
after the excision of dermoid in dogs. Veterinary Research
Communications 2009; 33: 1003–1012.
Griguer F, Raymond I, Regnier A. Preliminary evaluation of the
biocompatibility of the small intestinal submucosa in rabbit
cornea. Revue de Medecine Veterinaire 2001; 152: 597–604.
Schwarz C, Dang Burgener NP, Dosso AA. OCT Visante
observation of the progression of a perforated neurotrophic
cornea ulcer treated with amniotic membrane grafts. Journal
Francßais d’Ophtalmologie 2008; 31: 419–421.
Ramos JL, Li Y, Huang D. Clinical and research applications of
anterior segment optical coherence tomography – a review.
Clinical and Experimental Ophthalmology 2009; 37: 81–89.
Maeda N. Optical Coherence Tomography for corneal diseases.
Eye & Contact Lens 2010; 36: 254–259.
Wojtkowski M, Kaluzny B, Zawadzki RJ. New directions in
ophthalmic Optical Coherence Tomography. Optometry and
Vision Science 2012; 89: 524–542.
© 2013 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 17, 91–99