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British Journal of Ophthalmology, 1982, 66, 793-798
Combined posterior contusion and penetrating injury
in the pig eye. I. A natural history study
ZDENEK GREGOR
AND
STEPHEN J. RYAN
From the Department of Ophthalmology, University of Southern California,
Estelle Doheny Eye Foundation, Los Angeles, California, USA
SUMMARY We produced a standard experimental posterior contusion injury in the pig eye which
resulted in immediate intraocular haemorrhage and retinal whitening and folding without the
formation of a retinal break. When combined with a standard posterior penetrating eye injury,
traction retinal detachment began to develop after 2 weeks. We recognised a period of transition
between the resolution of the acute effects of contusion and the onset of fibrocellular proliferation
resulting from ocular penetration.
The damage from a penetrating eye injury results
from a combination of the effects of contusion and
laceration of ocular tissues. Posterior penetrating
injuries with a major contusive component may result
in far greater and more extensive damage than
those with laceration alone.' These injuries may be
complicated by an indirect scleral rupture or by
expulsive choroidal haemorrhage, with extrusion of
intraocular contents.2 Similarly haemorrhage, said to
originate from engorged choroidal vessels,3 may
occur during early vitrectomy performed on severely
injured eyes4 with little indication preoperatively of
the impending haemorrhage. Clinical impressions,
however, suggest that intraoperative haemorrhage is
less likely to occur if vitrectomy is delayed for several
days or weeks after a severe injury.
Previously developed experimental models of
posterior penetrating injury have reproducibly
resulted in vitreous traction and traction retinal
detachment.78 However, in these models ocular
penetration was achieved with a surgical type incision
only, and thus no contusive element, no choroidal
haemorrhage, and no intraoperative haemorrhage
from the uveal tract were encountered during
subsequent vitrectomies.9 '°
In an attempt to achieve a greater degree of clinical
relevance and the better to evaluate the timing of
vitrectomy after severe eye injury we decided to
investigate the role of contusion in posterior
penetrating injuries. The purpose of this study was to
record the natural history following a combined
posterior contusion and penetrating injury to the pig
eye.
Material and methods
The monkey eye was not considered suitable for the
purposes of this study because its sclera is very thin"
and the, impact necessary for significant ocular
contusion would have resulted in scleral rupture. We
selected the pig eye because its sclera is considerably
thicker. 2 The anatomy of the pig eye, including its
vitreous,"' has been said to resemble that of the
human eye in many respects, and the pig eye has been
the subject of a number of studies of anatomical'4-'7
and functional'8 changes following ocular contusion.
The major disadvantage of the pig as an experimental
animal is its rapid growth in size over the course of a
project lasting several months.
DEVELOPMENT OF STANDARD CONTUSION INJURY
To produce a contusion injury we used lead pellets
shot from a 022 calibre single shot pump pistol
(Model 132, Benjamin High Compression Air Pistol,
St Louis). The missile velocity (v) was measured on a
specially constructed bench connected to an electronic counter (Hewlett Packard 5228) and the mass
(m) of the missile determined by removing small
slices from the tip of a 0-22 calibre magnum lead
pellet. The measurements were done at the Department of Civil Engineering, University of Southemr
Correspondence to Stephen J. Ryan, MD, Estelle Doheny Eye California.
Foundation, 1355 San Pablo Street, Los Angeles, CA 90033, USA.
By our definition the standard posterior contusion
793
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Zdenek Gregor and Stephen J. Ryan
794
injury is an injury severe enough to produce intraocular haemorrhage but insufficient to result in
retinal dialysis. The optimal impact energy'9 required
to produce such an injury was determined empirically
both in 50 enucleated and in 20 live pig eyes. To
produce a standard posterior contusion injury as
described above an impact energy of 0-24 ft-lb (0-32
joule) was found satisfactory.
Thirty-three male and female domestic pigs (Sus
scrofa), aged 6-10 weeks and weighing 25 to 60
pounds (11-27 kg), were premedicated with a
mixture of ketamine, acepromazine, and atropine,
followed 10 minutes later by an injection of
fentanyl/droperidol (Innovar-Vet). Each animal was
anaesthetised by a mixture of halothane, nitrous
oxide, and oxygen administered via a nose cone. The
pupil of the right eye was dilated with drops of 1%
atropine sulphate, 10% phenylephrine, and 1 %
tropicamide. A retrobulbar injection of 4 ml of 2%
lignocaine was given to supplement anaesthesia and
to prevent retraction of the eye into the orbit. All
surgery was performed in sterile conditions under an
operating microscope.
A conjunctival peritomy was made temporally
from 7 to 11 o'clock and a fixation suture was placed
under the lateral rectus muscle. A standard contusion
injury was produced with a modified lead pellet
weighing 0 57 g travelling at a velocity of 33-3 m/s,
(impact energy, Ke=0-32 joule) from a hand-held
pistol. The pistol was held perpendicular to the sclera
at a distance of 2 5 cm. The limbal area and the ciliary
body including the pars plana were thus contused.
After contusion the impact site was inspected by
indirect ophthalmoscopy and scleral indentation to
rule out retinal breaks.
We then performed a standard posterior penetrating injury consisting of an incision 8 mm long
(from 8 to 10 o'clock) parallel to and positioned 2 5
mm from the corneoscleral limbus. The incision
through the pars plana avoided the lens and the
peripheral retina. The vitreous gel prolapsed and was
abscissed after gentle pressure on the globe. At times
difficulties were experienced in prolapsing vitreous
because the vitreous cortex of a young pig is more
solid than that of rabbits, monkeys, or humans. After
the removal of 0-3 to 04 ml of vitreous, the wound
was closed with 8-0 nylon sutures, with particular
attention paid to good wound apposition. After
wound closure the fundus, peripheral retina, and area
of the wound were examined with the indirect
ophthalmoscope and by scleral indentation to
confirm that no retinal damage had occurred.
Anterior chamber paracentesis was then performed.
In some eyes 0-5 ml of autologous blood, drawn
immediately beforehand, was injected via a 25 gauge
needle inserted under ophthalmoscopic control
Table I Design of the study
Group
No. of eves
I Standard posterior contusion injury
10
11 Standard posterior penetrating injury: with blood 5
5
with BSS
III Combined standard posterior contusion
and penetrating injury:
with blood 15
3
with BSS
Total
38
through the wound into the mid vitreous. In other
eyes 0 5 ml of balanced salt solution was injected. The
blood or balanced salt solution (BSS) was injected
slowly under low pressure in order to prevent reflux
through the wound. The conjunctiva was closed with
interrupted 7-0 Vicryl sutures, and a subconjunctival
injection of 20 mg of gentamicin was given.
All animals were followed up at weekly intervals
with indirect ophthalmoscopy and B-scan ultrasound
for up to 4 months after surgery. Findings were
recorded by drawings, descriptions, and/or photographs. Two animals died of unrelated causes during
follow-up.
In order to study the various components of a
combined posterior contusion and penetrating injury
the animals were divided into 3 groups (Table 1).
Ten eyes were subjected to a standard posterior
contusion injury without penetration; 5 of these eyes
were enucleated immediately after the injury and the
other 5 were enucleated at 4 months (group I). In 10
other eyes a standard posterior penetrating injury
without contusion was performed; 5 of these eyes had
an intravitreal injection of autologous blood and 5
received an intravitreal injection of balanced salt
solution (group II). All of these eyes were followed
up for 4 months before enucleation.
Group III contained 18 eyes that underwent a
combined posterior contusion and penetrating
injury. Fifteen of these received intravitreal injection
of blood and 3 control eyes received intravitreal
injection of BSS. All eyes in this group were
enucleated for histology at intervals between one day
and 4 months after injury.
Immediately after enucleation all the eyes were
fixed and examined carefully with the dissecting
microscope and by routine light microscopy.20
Results
GROUP I: STANDARD POSTERIOR CONTUSION
INJURY
Anterior segment. Less than one second after contusion the bulbar conjunctiva became intensely
hyperaemic. The pupil constricted by I to 2 mm, and
occasionally a small hyphaema developed within the
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Combined posterior contusion and penetrating injury in the pig eye. L. A natural history study
Table 2 Retinal detachment following combined
posterior injury
hyperaemia, but the anterior segment became quiet
one week after the injury. The cornea and the lens
Anterior circwnferential folds
Posterior radial folds
With blood
With BSS
With blood
With BSS
+++
++
+++
++
_
_
+
_
2
3
4
+
+
_
-
-
-
-
5
-
++
+++
+++
+++
-
++
_
-
Weeks
1
1'/2
8
10
14
16
-
+-
+++t
+
+
+
795
_
*Forward roll of ora.
tSubtotal retinal detachment.
next 5 minutes; this, however, resolved within the
first week. Lens changes were not observed in any of
the eyes studied.
A corneal epithelial abrasion of the temporal limbal
area resulted from the injury. This was slow to heal
and was frequently associated with prolonged stromal
oedema that usually cleared within 3 weeks.
Vitreous. A small vitreous haemorrhage overlying
the ora serrata was observed immediately after
contusion; this slowly increased during the next 5
minutes. Over the following 2 weeks the blood
became diffuse; it was resorbed a week later leaving
clear vitreous with no membrane or band formation.
Posterior vitreous detachment did not occur.
Retina. Immediately after contusion there was
widespread whitening and wrinkling of the retina
posterior to the impact site. This increased in
intensity and extent over the next 5 minutes, often
extending posteriorly to the equator. At the same
time circumferential haemorrhagic retinal folds
concentric with the injury site developed in the same
area. These gradually decreased in height and
disappeared during the second week of follow-up
(Table 2).
An extensive area of pigment epithelial change was
evident during the following week, with atrophy and
clumping extending as far as the equator; this was
particularly pronounced in the area where the retinal
folds had been iniitially noted. Further anteriorly,
pigment epithelial atrophy of the pars plana
developed in the immediate vicinity of the impact
site. The posterior retina appeared normal
throughout the duration of the study.
GROUP II: STANDARD POSTERIOR PENETRATING
INJURY
Anterior segment. After posterior penetrating injury
without contusion there was mild conjunctival
remained clear.
Vitreous. In the eyes with blood injection the view
of the posterior segment was obscured for 3 to 4
weeks. During this time the blood clot was at first
situated in the anterior vitreous cavity but subsequently became dispersed through the vitreous gel.
The clot was absorbed after 4 weeks, and, although
the vitreous remained hazy, posterior vitreous
separation was not evident. In 3 eyes transvitreal
strands spanned the distance between the posterior
retina and the site of the penetrating injury.
Retina. The retina became visible after 3 to 4
weeks; at that time, retinal folds were observed in the
posterior pole in all but one of the eyes. These folds
radiated from the disc towards the equator and
remained present throughout the follow-up period,
becoming less prominent in the later stages of the
study. Extensive retinal detachment did not occur.
No visible vitreous or retinal abnormalities were
observed in the eyes which were subjected to a
standard posterior penetrating injury plus an intravitreal injection of BSS. A rim of pigment epithelial
atrophy and a minimal amount of fibrous proliferation
developed around the site of the penetrating injury.
GROUP III: COMBINED STANDARD POSTERIOR
CONTUSION AND PENETRATING INJURY
Anterior segment. The appearance of the anterior
segment after injury was identical to that described in
the eyes in group I.
Vitreous. A small vitreous haemorrhage developed
immediately posterior to the contusion site. After the
penetrating injury but before the injection of blood
this haemorrhage increased considerably and became
more diffuse.
The 3 control eyes which had an injection of
physiological solution (BSS) at the time of injury
showed the same initial anterior retinal changes.
However, posterior retinal detachments did not
occur, and posterior vitreous separation and the
transvitreal bands were not observed.
After the injection of blood the view of the fundus
was obscured for various periods of time. At first the
blood clot was situated in the middle of the vitreous
cavity, but during the first week after injury the blood
began to diffuse through the vitreous gel, and at times
the clot, which condensed anteriorly, could be seen to
maintain its attachment to the disc.
By B-scan ultrasound examination the posterior
vitreous appeared to separate from the retinal surface
at about 11 days after the injury. However, between
the third and the fourth weeks, when the vitreous
became more clear, vitreous strands were seen
connecting the penetrating wound site and the retina
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Zdenek
796
Fig. I Gross section of an eve 6 days after the combined
contusion and penetrating injury. A dense blood clot is
situated posterior to the penetrating wound. Note anterior
circumferential retinalfold (black arrows) and early
anteroposterior bands (empty arrows). The posterior retina
is attached.
at the posterior pole. Between the fifth and eighth
weeks these vitreous strands were less prominent;
however, anterior vitreous condensations were
observed radiating from the penetrating wound site
behind the lens.
Retina. Immediately after contusion a small haemorrhage covered the ora serrata posterior to the
impact site, and widespread whitening and wrinkling
of the adjacent peripheral retina occurred. This
Fig. 2 Gross section of an eye 4 weeks after a combined
contusion and penetrating injury. High posterior retinalfolds
are drawn towards the penetrating wound by transvitreal
traction bands. The anterior circumferential retinal folds are
no longer present.
Gregor and Stephen J. Ryan
increased in intensity and extent following the
penetrating component of the injury, often reaching
the posterior pole. Concurrently, circumferential
folds developed in the equatorial and anterior retina
associated with subretinal haemorrhage. These
localised subretinal haemorrhages persisted until the
seventeenth day after injury (Fig. 1).
In eyes enucleated at 8 days after injury fullthickness retinal folds appeared at the posterior pole.
These were arranged in a radial fashion, and vitreous
strands connected the tips of the folds to the site of
the penetrating wound (Fig. 2). The posterior radial
folds persisted throughout the period of the followup, even though the transvitreal strands became less
prominent. In the late stages of follow-up small
peripheral retinal detachments occurred in the form
of a forward roll of the ora serrata onto the pars plana
1800 from the injury site (Table 2). Extensive retinal
detachment did not develop, though subtotal detachment did occur in one eye.
Discussion
In this study we attempted to investigate the contusive
component of a severe penetrating eye injury. Others
have documented the effects of a contusion injury
alone, but our aim was to examine how the combination of contusion and penetration relate to the
development of intraocular haemorrhage.
In clinical practice the overall picture after ocular
contusion is that of retinal opacification,2' 22 retinal
break formation, 14 23 24 and haemorrhage from
choroidal vessels.24 Blood accumulates in the suprachoroidal space as well as under the retina and may
gain access to the vitreous cavity.2425 Haemorrhage
may result from direct rupture of choroidal vessels or
may follow capillary dilatation secondary to tissue
anoxia caused by initial vasoconstriction.' In this
study the standard contusive injury was designed to
produce choroidal vascular changes and haemorrhage
without producing a retinal break, and, despite the
relatively low kinetic energy which we used, subretinal and vitreous haemorrhage was consistently
present in the area of the injury.
The vitreoretinal changes following our standard
contusion injury were similar to those usually seen
clinically and to those described in previous
experiments.24 Retinal whitening and wrinkling
adjacent to the site of the impact were a constant
feature. Interestingly, the retinal opacification
appeared more pronounced and extensive after the
combined injury (group III) than after contusion
alone (group I); this may have been due to the sudden
lowering of intraocular pressure or to a delay in the
observation time or both.
The circumferential retinal folding posterior to the
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Combined posterior contusion and penetrating injury in the pig eye. I. A natural history study
contusion site resembled that observed previously by
Cox in association with anterior retinal dissolution,24
even though in our model fragmentation of the retina
did not occur. Although no large haemorrhagic
choroidal detachments developed, the presence of
subretinal haemorrhage beneath the anterior circumferential retinal folds indicated bleeding from the
choroid. -Similarly, since no breaks in the retinal
vessels were evident, the vitreous haemorrhage
adjacent to the impact site was assumed to have
originated from the uveal tract. As in the clinical
setting, the vitreous haemorrhage gradually became
absorbed and the localised retinal detachment
settled; this was accompanied by localised proliferation of the retinal pigment epithelium in the
areas of contusion.
In the pig eye, unlike the monkey eye, total retinal
detachment did not develop after a standard
posterior penetrating injury with blood injection.
The retinal folds in the pig eye were frequently
extensive but remained localised to the posterior
pole, although accompanied by signs of anteroposterior vitreous traction; such a situation is unusual
in man and was not observed in the rhesus monkey
eye. ' However, anteroposterior vitreous traction
and localised detachment of the posterior retina have
been previously described in the rabbit eye after an
experimental injury26 as well as following injection of
retinal pigment epithelial cells into the vitreous.27
Significantly, posterior vitreous detachment does not
occur in the rabbit eye after a posterior penetrating
injury.26 The apparent lack of posterior vitreous
separation in the pig eye was subsequently confirmed
on histological examination.28 In pig eyes with the
combined contusion and penetrating injury, without
intravitreal blood injection, vitreoretinal traction or
traction retinal detachment did not occur.
Changes secondary to contusion were obvious
immediately. These changes persisted for less than 2
weeks, whereas the tractional complications of the
penetrating injury did not become clinically apparent
until the second week after the injury. Indeed, there
appeared to be a period of transition between
resolution of the effects of contusion and the onset of
complications of the penetrating injury. The former
was shown by the disappearance of retinal opacification and the spontaneous reattachment of localised
anterior retinal detachment; the latter was characterised by the development of transvitreal strands,
localised posterior retinal detachment, and, in the
late stages, anterior roll of the ora serrata located 1800
opposite the penetrating injury site. Secondary
haemorrhage did not occur in any of the animals in
this part of the study.
The results of this study support clinical observations on the haemorrhagic effects of the contusive
79^7
component of a severe penetrating injury. It is
recognised that intraocular haemorrhage due to
contusion occurs at the time of injury but may also
occur during a very early vitrectomy. From this study
it would seem that by the second week after injury
haemorrhage due to contusion and the accompanying
choroidal changes begins to abate. This may be an
interval of time during which the effects of contusion
subside and the tractional complications of the
penetrating component have not yet become
irreversible. It is therefore possible that in this model,
if vitrectomy is performed during this period, traction
retinal detachment may still be prevented and yet the
potentially disastrous operative haemorrhage may be
avoided.
As a result of this experiment we obtained a useful
model with clinical evidence of vitreoretinal traction
which will be used for a controlled trial of vitrectomy
in the treatment of experimental combined contusive
and penetrating posterior eye injury.
We thank Kate Borkowski and her colleagues for technical assistance
and Sue Gertson for secretarial help.
This study was supported in part by NIH grants EY 02061 and EY
03040 (Dr Ryan).
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Combined posterior contusion and
penetrating injury in the pig eye. I. A
natural history study.
Z Gregor and S J Ryan
Br J Ophthalmol 1982 66: 793-798
doi: 10.1136/bjo.66.12.793
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