—  SHORT COURSE  —

OPHTHALMIC PATHOLOGY FOR THE NON-SPECIALIST


CASE 8 – PENETRATING OCULAR TRAUMA

J. Godfrey Heathcote, M.B.,Ph.D.  —  Janice R. Safneck, M.D.




History
An 87-year-old woman fell and hit her right eye on the corner of her dresser.

Diagnosis
Limbal rupture resulting from blunt trauma
a)loss of iris and lens
b)massive intraocular hemorrhage
c)ciliary body detachment and prolapse
d)retinal and choroidal detachment
e)partial tearing of optic nerve
f)reactive acute inflammation

Histopathology
The globe is slightly collapsed, displaying rupture at the limbus superiorly with reddish material protruding from the wound. Blood is visible through the wrinkled cornea. Opening the eye reveals abundant intraocular hemorrhage. No lens is visible. Blood is present within the wound.


Case 8, Slide 19 - Penetrating Ocular Trauma: Front view of a partially collapsed globe displaying rupture at the limbus superiorly with reddish material protruding from the wound. Blood is visible through the wrinkled cornea.
Case 8, Slide 20 - Penetrating Ocular Trauma: Cut surface of eye revealing abundant intraocular hemorrhage beneath partially detached ciliary body, retina and choroid. No lens is visible. Blood is present within the wound.
Case 8, Slide 21 - Penetrating Ocular Trauma: Photomicrograph of limbal rupture with ciliary body protruding through the defect.

Microscopically, limbal rupture is confirmed with ciliary body protruding through the defect. No portions of lens or iris are encountered. There is massive intraocular hemorrhage beneath choroid, with choroidal detachment, and within conjunctiva, trabecular meshwork, canal of Schlemm, ciliary body, and optic nerve. Cyclodialysis, retinal detachment and focal partial tearing of the optic nerve head are seen. Acute inflammation is abundant within choroid and can also be noted in cornea and sclera. Other findings include a break in Descemet's membrane and cystoid degeneration of peripheral retina.

Discussion
Ocular injuries have wide variations in clinical presentation, cause and visual outcome and trauma is a leading cause of visual impairment. In the USA alone, 2.4 million eye injuries occur per year, 68,000 of them vision-threatening.1  Most are unilateral. World-wide, eye injuries have resulted in 19 million people with unilateral vision loss, 2.3 million with bilateral visual impairment, and 1.6 million blind.2 

The most serious injuries generally involve disruption of the eye. Such injuries happen at a rate of 3.81/100,000 in USA and the majority of affected individuals are males less than age 40.1  However, there is another peak in incidence above age 70 affecting men and women equally.3  Common settings for serious eye injuries include home, work place, assault and recreational/outdoor activities.4  The percentage of injuries in each situation varies with the population studied; however, in the United States and Great Britain, the home is where the largest proportion of serious ocular trauma occurs, as mandatory eye protection in hazardous workplaces, eye protective devices for various sports, and regulations governing glass in windshields have reduced injury in these settings.2,5  Assaults and motor vehicle crashes are more likely in younger individuals while older patients frequently have ocular injuries related to falls.3 

Both sharp objects, e.g. broken glass, knives and sharp metal pieces,4  and blunt trauma,6  contribute to injury. Strictly speaking, the term "ruptured" globe refers to a full thickness wound caused by a blunt object, "laceration" a full thickness wound caused by a sharp object, "penetrating" injury a single full thickness wound typically the result of a sharp object, and "perforating" injury two full thickness wounds, entrance and exit, caused by the same agent. Contusions are closed globe injuries caused by blunt objects. Good visual outcome is associated with initial visual acuity of 20/200 or better, anterior wound, wound length <10 mm, and sharp injury.7  The percentage of open globe injuries ultimately requiring enucleation varies in relation to cause with an overall figure around 11%.4  Reasons for enucleation include loss of vision, fear of sympathetic ophthalmia, pain and unsightliness. Indeed, in an American study of over 24,000 surgical specimens seen over a 55 year period in an eye pathology laboratory, ocular trauma was the most common underlying condition resulting in surgical enucleation (40.9%) from the 1940's up to the present time.8  The mechanisms of injury in such eyes were most commonly penetration (42.2%), followed by contusion (26.7%), rupture (17.0%) and perforation (3.0%).8 

Assault-related penetrating ocular injuries vary from 1-53% in reported series, typically affecting men age 20-40. Alcohol consumption and/or illicit drug use are factors in 50-70% of cases.9,10  The ocular injury is frequently part of multiple trauma. Injury mechanisms include projectiles (bullets, buckshot), sharp objects (glass, knives) and blunt objects (especially fists).9,10  Posterior segment injuries occur in 70% and visual prognosis is poor. A higher proportion of left eyes is injured, likely because most assailants are right-handed and thus hit the victim's left face.9 

Blast fragmentation ocular injuries are frequent in military personnel. Unlike other forms of ocular trauma, 15-25% are bilateral. Open and closed globe injuries affect both anterior and posterior segments. Endophthalmitis is slightly more common than after civilian trauma; 20% involve Bacillus sp and are aggressive infections with a poor visual prognosis.11  The incidence of work-related ocular injuries ranges between 8-70%, generally affecting men less than age 40 working in construction, manufacturing and agriculture. Most injuries are due to projectiles, particularly metal fragments but sometimes wood, with a smaller number caused by chemicals. Anterior segment injuries occur in 93%, posterior segment trauma in 63% and 3-4% require enucleations.4,12  Thermal and chemical burns typically affect anterior structures and only occasionally require enucleation. Eyelid burns with subsequent contractures are the most frequent, with corneal abrasions and burns, foreign bodies, conjunctival burns and inflammation and cataracts also reported.13 

Motor vehicle accidents are responsible for 3.4-30% of traumatic ocular injuries with a roughly equal gender distribution. Typically the anterior segment is penetrated by glass fragments and enucleation rates range from 0-23%.14  Sport-related injury varies from 2-23%, affecting predominantly men; BB/pellet guns, baseball, fishing and hockey cause the most injuries. Damage is most severe posteriorly, frequently leading to visual loss and enucleation rates of more than 50%.4,15,16 

Macroscopic and microscopic findings
Gross examination of a traumatized eye enucleated within several weeks of injury often reveals a corneal or scleral wound(s), typically longer than 10 mm.17  The globe may be normal in size or partially collapsed, depending on the severity of trauma and if surgical repair was performed. Sharp objects forcefully hitting the eye can cut through cornea and/or sclera, and sometimes exit the eye. Sites of rupture in blunt trauma injuries typically correspond to areas of anatomic scleral thinning at the limbus, just posterior to the rectus muscle insertions, at the equator and at the lamina cribrosa; sites of previous surgery also are weak points.18  Blood and tissue may protrude through the wound. If surgical repair was attempted, fine sutures may be visible. Blood may be seen in episcleral tissues, may be visible intraocularly through the cornea (blood in the anterior chamber is termed hyphema) and occasionally, may be evident within and around the optic nerve. Opening eye typically reveals loss or partial loss of lens, iris and ciliary body, retinal and choroidal detachments, and hemorrhage.17,19  A foreign body may be found.

Microscopic examination reveals loss or partial/total necrosis of iris, and complete or partial loss or dislocation of lens. Hemorrhage is usually prominent anteriorly, within vitreous cavity, subretinally and beneath uveal tract. Ciliary body may be partially or completely detached, the latter termed cyclodialysis. The retina is usually detached except for its attachment at the optic nerve head; occasionally it may have been expelled from the eye by hemorrhage or may be present without any attachment. Choroidal detachment is frequent and vitreous base avulsion also may be seen. Approximately one-third of cases show poor wound apposition and more than half display incarcerated tissues in the wound, typically uvea and vitreous, sometimes portions of lens and retina.20  Typically, a reactive uveitis is present; initially polymorphs are prominent but lymphocytes increase with time.17,19 

Histological changes associated with blunt trauma also include commotio retinae, choroidal rupture, macular hole and optic nerve avulsion.21  Commotio retinae consists of intraretinal pigment, disruption of photoreceptor outer segments and damage to the retinal pigment epithelium. Choroidal ruptures occur parallel to the ora serrata or in a curvilinear fashion around the disc margin; usually they are accompanied by subretinal hemorrhage and sometimes by intrachoroidal and vitreous hemorrhage. The lesion heals by scarring with hyperpigmentation and sometimes neovascularization; overlying retina may exhibit atrophy. Traumatic macular holes result from cystoid macular edema with cyst coalescence leading to partial retinal rupture and ultimately a full thickness hole. Complete or partial avulsion of the optic nerve (traumatic separation of the optic nerve from the globe at the lamina cribrosa with or without a break in the optic nerve sheath or adjacent sclera) can occur after blunt or penetrating trauma.22  Ultimately, fibrovascular or gliotic tissue may partially or completely replace the optic nerve head and extend into vitreous.

Approximately 9 days post-trauma, fibrous proliferation becomes evident, typically originating in the wound with inward extension.19  By one month, fibrovascular membranes may involve vitreous, surround lens remnants and attach to ciliary body and retina. Epiretinal and subretinal membranes are seen in approximately half of cases.20  Hemosiderin can be identified approximately 1 week after trauma and is marked by one month, commonly deposited in choroid and ciliary body and sometimes in cornea.19 

Other consequences include traumatic cataract, glaucoma, and endophthalmitis. Traumatic cataract develops in 1-15% of ocular injury by various mechanisms.23  The lens capsule may become compromised with lens epithelial cells responding by forming a fibrous plaque. Iris pigment may be pressed onto the anterior lens capsule and may be associated with underlying punctate opacities. Penetrating injuries can produce capsular disruption with aqueous exposure to inner lens resulting in complete opacification or rarely, resorption.23  Phacoanaphylactic endophthalmitis may also occur.24  The lens may become cataractous as a result of a retained intraocular foreign body; iron may be deposited on the lens while copper generally produces much inflammation unless it is sequestered in the lens. Post-traumatic uveitis can lead to cataract formation. Ultimately an injured eye may become phthisical.

Glaucoma post-trauma can be caused by disruption of the trabecular meshwork, angle recession, inflammation, peripheral anterior synechiae, fibrous and/or epithelial downgrowth covering angle structures, dislocation of the lens and leakage of lens material from disrupted lens with or without cataract (phacolytic glaucoma). Although ocular trauma is relatively frequent, subsequent infection is uncommon. Staphylococcus epidermidis, Staphylococcus aureus, Streptococcal sp. and Bacillus sp. are typical pathogens. Bacillus sp. often are associated with penetrating injuries from metallic objects and can result in rapid ocular destruction.

Trauma-related changes often are seen in surgical specimens but also can be identified in globes removed post-mortem. One particular specialized area of ocular trauma involves eye examination in suspected child abuse. Injuries may be multiple, at different stages, and accompanied by cerebral damage. The earliest intraocular injuries are focal subhyaloid hemorrhages and retinal detachment particularly near the ora serrata.25  Optic nerve sheath hemorrhage, especially subdural, is common26  and frequently is associated with, but is not the result of, subdural intra-cranial hemorrhage.25,27  In order to adequately visualize the orbital nerve, the eye is best removed using the posterior approach via the cranial cavity (removal of the orbital roof through the skull base).28  Other retinal injuries include retinoschisis (retinal splitting), perimacular retinal folds, and multilayered retinal hemorrhages,29  which may be widespread and severe, or small, scattered and focal.27  As well, there may be vitreous, subretinal and preretinal hemorrhages, iridodialysis, subluxed or dislocated lens and papilloedema as well as periorbital hematoma, eyelid laceration and subconjunctival hemorrhage.25  The presence of hemosiderin-laden macrophages intraocularly may relate to time of death after injury and does not necessarily imply multiple episodes of trauma.26  Other causes of retinal hemorrhages in infants include birth trauma, cardiopulmonary resuscitation, asphyxia, seizures, hematological disorders and ruptured cerebral aneurysm/vascular malformation.25,26  While the ocular findings outlined above can be useful in distinguishing traumatic from non-traumatic deaths, they cannot separate accidental from non-accidental injury. Thus interpretation of ocular findings in children at post-mortem requires careful correlation with history, clinical data and other autopsy findings as well as considerable experience.

Sympathetic Ophthalmia
Sympathetic ophthalmia is a bilateral, uveal granulomatous disease following unilateral penetrating ocular injuries, either traumatic or surgical. The injured eye is referred to as the exciting or inciting eye, the other globe as the sympathizing eye. The cause of sympathetic ophthalmia is unknown but it appears to be an autoimmune response to previously sequestered uveal antigens, possibly the MART-1 peptide of melanocytes, in genetically predisposed individuals.30 

Sympathetic ophthalmia is rare today, with an incidence of 0.28 - 1.9% after penetrating ocular trauma and 0.01 - 0.05% after surgery.30  Clinicopathological review of sympathetic ophthalmia cases shows just over 50% are secondary to trauma and the remainder related to surgery.30,31  Occasional instances occur after perforating corneal ulcers and in association with malignant melanomas having extrascleral extension or after irradiation treatment. Most surgical procedures implicated in sympathetic ophthalmia involve eye penetration but laser cyclocryotherapy, an externally administered treatment, also can produce sympathetic ophthalmia. The interval between injury and the onset of sympathetic ophthalmia is typically between 2 weeks to 2 months with 90% of cases occurring within one year but the interval may range from 5 days to 66 years.30 

Histologically, there is panuveitic non-necrotizing granulomatous inflammation accompanied by Dalen-Fuchs nodules which are collections of cells between Bruch's membrane and the retinal pigment epithelium. Epithelioid cells ingesting pigment often are seen. Dalen-Fuchs nodules while characteristic of sympathetic ophthalmia are not pathognomonic of it and may be found in sarcoidosis, tuberculosis and Vogt-Koyanagi-Harada syndrome.32  Classical sympathetic ophthalmia displays granulomas surrounded by T-lymphocytes throughout the uveal tract. Although plasma cells are supposed to make up only a small percentage of the inflammatory infiltrate, they may be present in substantial numbers. In approximately 40% of eyes with sympathetic ophthalmia, eosinophils are scattered throughout the uveal tract but neutrophils are not a feature of sympathetic ophthalmia.31,33  Involvement of the choriocapillaris (traditionally said to be spared) has been reported in 40-100% of cases and chorioretinal scarring in 7-25%.34  Inflammation may be present in the optic nerve beyond the lamina cribrosa and in meninges. Phacoanaphylactic endophthalmitis may be associated with sympathetic ophthalmia.

Histologic differential diagnosis of classical sympathetic ophthalmia includes sarcoidosis, infections such as tuberculosis and Vogt-Koyanagi-Harada syndrome. A history compatible with sympathetic ophthalmia is critical since the diagnosis cannot be based on histologic findings alone. It should be noted that occasional granulomas may be found in eyes enucleated post-trauma but with no history of sympathetic ophthalmia.35  Treatment of sympathetic ophthalmia consists of steroid therapy and, in poorly responding cases, immunosuppressive drugs such as cyclosporin, azathioprine, methotrexate, cyclophosphamide and chlorambucil. It has been noted that if a traumatized eye is removed within 2 weeks of injury, the risk of sympathetic ophthalmia is very small. Nonetheless, because sympathetic ophthalmia is rare and because the injured eye may become the eye with better vision, it is common practice to try to save the injured eye if there is any potential for useful vision.30  Whether or not there is any benefit in removing the exciting eye once sympathetic ophthalmia has developed is matter of considerable controversy.

References

  1. Parver LM, et al: Characteristics and causes of penetrating eye injuries reported to the National Eye Trauma Registry, 1985-1991. Pub Health Rep 1993;108:625-632.
  2. MacEwen CJ: Ocular injuries. J R Coll Surg Edinb 1999;317-323,
  3. Tielsch JM: Frequency and consequences of ocular trauma. A population perspective. Ophthalmol Clin N A 1995;8:559-567.
  4. Dunn ES, et al: The epidemiology of ruptured globes. Ann Ophthalmol 1992;24:405-410.
  5. May DR, et al: The epidemiology of serious eye injuries from the united States Eye Injury Registry. Graefe's Arch Clin Exp Ophthalmol 2000;238:153-157.
  6. Liggett PE , et al: Ocular trauma in an urban population. Review of 1132 cases. Ophthalmology 1990;97:581-584.
  7. Esmaeli B, et al: Visual outcome and ocular survival after penetrating trauma. A clinicopathologic study. Ophthalmology 1995;102:393-400.
  8. Spraul CW, Grossniklaus HE: Analysis of 24,444 surgical specimens accessioned over 55 years in an ophthalmic pathology laboratory. Int Ophthalmol 1998;21:283-304.
  9. Dannenberg AL, Parver LM, Fowler CJ: Penetrating eye injuries related to assault. The National Eye Trauma System Registry. Arch Ophthalmol 1992;110:849-852.
  10. Groessl S, Nanda SK, Mieler WF: Assault-related penetrating ocular injury. Am J Ophthalmol 1993;116:26-33.
  11. Wong TY, Seet B, Ang C-L: Eye injuries in twentieth century warfare: a historical perspective. Surv Ophthalmol 1997;41:433-459.
  12. Dannenberg AL, et al: Penetrating eye injuries in the workplace. The National Eye Trauma System Registry. Arch Ophthalmol 1992;110:643-648.
  13. Stern JD, Goldfarb IW, Slater H: Ophthalmological complications as a manifestation of burn injury. Burns 1996;22:135-136.
  14. Nanda SK, Meiler WF, Murphy ML: Penetrating ocular injuries secondary to motor vehicle accidents. Ophthalmology 1993;100:201-207.
  15. Fountain TR, Albert DM: The histopathology of sports-related ocular trauma, 1980-1986. Int Ophthalmol Clin 1988;28:206-210.
  16. Sternberg P Jr, et al: Ocular BB injuries. Ophthalmology 1984;91:1269-1277.
  17. Freitag SK, et al: An epidemiologic and pathologic study of globes enucleated following trauma. Ophthalmic Surg 1992;23:409-413.
  18. Pieramici DJ, Parver LM: A mechanistic approach to ocular trauma. Ophthalmol Clin N A 1995;8:569-587.
  19. Punnonen E: Pathological findings in eye enucleated because of perforating injury. Acta Ophthalmol 1990;68:265-269.
  20. Winthrop SR, et al: Penetrating eye injuries: a histopathological review. Br J Ophthalmol 1980;64:809-817.
  21. Elliot D, Avery RL: Nonpenetrating posterior segment trauma. Ophthalmol Clin N A 1995;8:647-666.
  22. Sanborn GE, et al: Evulsion of the optic nerve: a clinicopathological study. Can J Ophthalmol 1984;19:10-16.
  23. Cohen A, Hersh PS, Fleischman JA: Management of trauma-induced cataracts. Ophthalmol Clin N A 1995;8:633-646.
  24. Perlman EM, Albert DM: Clinically unsuspected phacoanaphylaxis after ocular trauma. Arch Ophthalmol 1977;95:244-246.
  25. Green MA, et al: Ocular and cerebral trauma in non-accidental injury in infancy: underlying mechanisms and implications for paediatric practice. Br J Ophthalmol 1996;80:282-287.
  26. Budenz DL, et al: Ocular and optic nerve hemorrhages in abused infants with intracranial injuries. Ophthalmology 1994;101:559-565.
  27. Riffenburgh RS, Sathyavagiswaran L: Ocular findings at autopsy of child abuse victims. Ophthalmology 1991;98:1519-1524.
  28. Parsons MA, Start RD: Necropsy techniques in ophthalmic pathology. J Clin Pathol 2001;54:417-427.
  29. Elner SG, et al: Ocular and associated systemic findings in suspected child abuse. a necropsy study. Arch Ophthalmol 1990;108:1094-1101.
  30. Gasch AT, et al: Postoperative sympathetic ophthalmia. Int Ophthalmol Clin 2000;40:69-84.
  31. Lubin JR, Albert DM, Weinstein M: Sixty-five years of sympathetic ophthalmia. A clinicopathologic review of 105 cases (1913-1978) Ophthalmology 1980;87:109-121.
  32. Reynard M, Riffenburgh RS, Minckler DS: Morphological variation of Dalén-Fuchs nodules in sympathetic ophthalmia. Br J Ophthalmol 1985;69:197-201.
  33. Chan C-C, et al: 32 cases of sympathetic ophthalmia. A retrospective study at the National Eye Institute, Bethesda, Md, from 1982-1992. Arch Ophthalmol 1995;113:597-600.
  34. Chan C-C: Relationship between sympathetic ophthalmia, phacoanaphylactic endophthalmitis, and Vogt-Koyanagi-Harada disease. Ophthalmology 1988;95:619-624.
  35. Wilson, MW, Grossniklaus HE, Heathcote JG: Focal posttraumatic choroidal granulomatous inflammation. Am J Ophthalmol 1996;121:397-404.