Diagnostic and Therapeutic Challenges
Edited by H. Richard McDonald
Drs. Steven J. Ryder, Cristiano Oliveira, Marc J. Dinkin, Donald J. D’Amico, Anton Orlin, and Sara J. Haug
T
after a routine soccer ball heading. Although there had been head strikes against the ball during the game, there were no direct contusions to the eye, body collisions, or falls. Presenting visual acuity in the left eye was no light perception, and fundus photography revealed a cherry red spot with vascular attenuation and segmentation of the blood column within the vessels, indicating retrograde perfusion (Figure 2). Optical coherence tomography showed increased hyperreflectivity of the inner retinal layers (Figure 3), and a CRAO was confirmed by fluorescein angiography (Figures 4–6). Sports injuries constitute a large portion of traumatic injuries to eyes, particularly among children and young adults.1,2 In the past, it was believed that injury to the globe is rarely caused by balls larger than 4 inches in diameter given the protective effect of the bony orbit. Therefore soccer, with its larger diameter ball, was less likely to cause significant injury. A number of studies have shown this not to be the case; in fact, soccerrelated eye injuries can result in more severe injury than previously recognized with poor visual outcomes.1–3 One case series of 13 soccer-related ocular injuries found final Snellen visual acuity was 20/200 or worse in a quarter of those studied.1 A series of experiments published in 2004 suggest that the mechanism of ocular injury from soccer balls involves deformation of the ball on impact, which allows a small “knuckle” of the ball to enter the orbit and impact the globe.3,4 The authors also found that the time the soccer ball spends in the orbit is longer than other projectiles and there is a secondary suction effect produced on the orbital contents during rebound of the ball. This suction component increases the distortion of the ocular anatomy, which can lead to more severe injuries.4 There is only one case in the literature describing a CRAO after a soccer ball injury.5 In that case, there was direct trauma to the orbit by the soccer ball, in
his case is submitted by Drs. Steven J. Ryder, Cristiano Oliveira, Marc J. Dinkin, Donald J. D’Amico, and Anton Orlin, of the Department of Ophthalmology, Weill Cornell Medical College, New York, New York; commented by Dr. Sara J. Haug, San Francisco, California. Case Report
An 18-year-old healthy white male presented to our retina clinic within 90 minutes of first noticing visual loss in his left eye while playing soccer, soon after a routine soccer ball heading. Throughout the game, there were prior head strikes against the soccer ball but no head-to-head or body collisions or falls. He denied focal neurologic symptoms, headache, or other visual symptoms. There was a history of previous “multiple” concussions not only from collisions during a soccer game but also in the setting of a motor vehicle accident 3 months before the present incident. His general history was otherwise negative, specifically, no medications or illicit drug use. Visual acuity at presentation was 20/20 in the right eye and no light perception in the left eye, with a marked left relative afferent pupillary defect. Intraocular pressure was 15 mmHg in each eye. Slit-lamp examination was normal in both eyes, with no iritis or periorbital swelling. Dilated funduscopic examination was normal in the right eye (Figure 1) and remarkable for mild optic nerve swelling, retinal vascular attenuation with box-carring, and a macular cherry red spot consistent with a central retinal artery occlusion (CRAO) in the left eye (Figure 2); no arterial embolus was observed. Optical coherence tomography (OCT) of the left eye revealed increased hyperreflectivity of the inner retina with loss of architecture (Figure 3). The fluorescein angiography revealed absent retinal perfusion confirming the central retinal arterial occlusion (Figures 4–6 transit time of 18 seconds, 50 seconds, and 3 minutes 16 seconds, respectively). This case is presented for discussion regarding pathogenesis and management.
Dr. Sara J. Haug (San Francisco, California): Dr. Ryder et al present the case of an 18-year-old man with a history of multiple concussions who suffered complete vision loss while playing soccer 221
222
RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2016 VOLUME 36 NUMBER 1
Fig. 1. Color fundus photography of right eye at initial presentation is unremarkable.
contrast to the case presented here, which did not have direct ocular trauma from the soccer ball before the arterial occlusion. In addition to the CRAO, other signs of trauma including commotio retinae were observed. Despite the direct impact of the soccer ball on the orbit, imaging and laboratory work-up were negative, and the authors concluded the CRAO was likely due to arterial vasospasm. The most common cause for a CRAO is atherosclerotic disease of the internal carotid artery in an elderly patient resulting in embolic occlusion of the artery. However, a number of case reports identify trauma as the etiology behind the arterial obstruction. Often, this can be seen in conjunction with other pathology, such as systemic lupus erythematosus, hemoglobinopathies, or coagulation abnormalities, but systemic pathology
Fig. 2. Color fundus photography of left eye at presentation.
is not noted in all cases of traumatic CRAO.6–11 One proposed mechanism by which trauma can lead to a CRAO in cases of concussion or closed-eye head trauma is compression of the central retinal artery induced either by a hematoma, by air in the case of orbital emphysema or by raised intraorbital pressure from soft tissue swelling, resulting in arterial occlusion. Other postulated theories of traumatic CRAO in concussive head injuries include arterial vasospasm or sheering injury from traumatic rotation of the globe. Common to these conditions is damage to the endothelial cells of the artery with exposure of the subintimal tissue to the bloodstream, which can then stimulate platelet aggregation and thrombus formation.8–10 It has also been proposed that activation of the complement cascade, which can occur in concussive head trauma, can lead to vascular occlusion. Specifically, Complement Factor 5 activation leads to neutrophil activation, increased expression of adhesion molecules, emigration of neutrophils and chemotaxis, monocyte activation, and mast cell degranulation, resulting in vascular constriction. Studies done in a cat model confirm this hypothesis by demonstrating transient occlusion of retinal arterioles induced by intravascular complement activation.7 In the case presented here by Dr. Ryder et al, there was no direct ocular trauma with the soccer ball. However, the patient’s history of multiple concussions may have predisposed the patient to an arterial occlusion due to cumulative vascular damage, even with relatively minor trauma. The impact of the head on the soccer ball may have been enough to induce arterial vasospasm or sheering injury, leading to a CRAO. However, it is also possible that the soccer ball heading has nothing to do with the CRAO experienced by our patient, and this is a nontraumatic CRAO, which has a broad differential diagnosis in a young person. Excluding a traumatic cause, the differential diagnosis in our patient includes cardiac valvular disease, embolic disease, hypertension, and vasculitis. Autoimmune disorders, such as systemic lupus erythematosus, polyarteritis nodosa, and Behcet disease, also predispose a patient to arterial occlusions. Conditions leading to hypercoagulability are also on the differential, such as hyperhomocysteinemia, hyperlipidemia, anticardiolipin antibody, antiphospholipid antibody, antithrombin III mutation, polycythemia, Factor V Leiden, activated Protein C resistance, Protein C or S deficiency, oral contraceptive use, and pregnancy. Carotid artery dissection, stroke, and intracranial hemorrhage must also be considered. Work-up for this patient must include a thorough medical history and contrast-enhanced magnetic resonance imaging of the brain and orbits, magnetic
DIAGNOSTIC AND THERAPEUTIC CHALLENGES
223
Fig. 3. Optical coherence tomography of the left eye at initial presentation revealed increased hyperreflectivity of the inner retina with loss of architecture.
resonance angiogram of the head and neck, and magnetic resonance venogram of the head to evaluate for intracranial hemorrhage, infarct, and carotid dissection. An echocardiogram must be performed to rule out cardiac valvular disease such as an atrial myxoma or endocarditis, and electrocardiogram testing should also be performed to evaluate for cardiac arrhythmia. Laboratory tests for hypercoagulability must be sent and a complete blood count and electrolyte work-up. Management of a CRAO has largely been supportive with very few options to improve outcomes. Treatment options, such as acetazolamide infusion, carbogen inhalation, hemodilution, ocular massage, and paracentesis, as well as vasodilators, such as intravenous glyceryl trinitrate, have not been shown to alter the natural history of a CRAO. More recent evidence suggests that hyperbaric oxygen treatments may improve final visual acuity in some patients.12,13
Animal studies have shown that hyperbaric oxygen treatment initiated immediately after arterial occlusion can reduce retinal neuronal apoptosis.13 A retrospective study by Dr. Menzel-Severing et al compared hyperbaric oxygen treatment in patients with CRAO to patients receiving hemodilution only. They found that patients receiving hyperbaric oxygen treatments had a trend toward better visual outcomes compared with hemodilution alone, but this was not statistically significant and some patients did not respond to any treatment.12 A randomized prospective study is necessary to further evaluate hyperbaric oxygen treatment in cases of retinal artery occlusion.
Fig. 4. Fluorescein angiography at initial presentation revealed absent retinal perfusion at transit time of 18 seconds.
Fig. 5. Fluorescein angiography at initial presentation revealed absent retinal perfusion at transit time of 15 seconds and 3 minutes.
Editor’s Note: Drs. Ryder, Oliveira, Dinkin, D’Amico, and Orlin have presented an 18-year-old male with CRAO after a routine soccer ball heading without direct ocular trauma. The patient is presented for discussion of
224
RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2016 VOLUME 36 NUMBER 1
Fig. 8. Fluorescein angiography at 1-day follow-up illustrating reperfusion of retinal vasculature.
Fig. 6. Fluorescein angiography at initial presentation revealed absent retinal perfusion at transit time of 16 seconds.
pathogenesis and management of CRAO in a patient with multiple previous concussions. Dr. Sara Haug has consulted and provided us with a differential diagnosis of nontraumatic CRAO in a young person. 1. Cardiac • Valvular disease • Embolic disease • Hypertension
2. Autoimmune • Lupus • Polyarteritis nodosa • Bechet’s disease 3. Hypercoagulability • Hyperhomocysteinemia • Hyperlipidemia • Anticardiolipin antibody • Antiphospholipid antibody • Antithrombin III mutation • Polycythemia • Factor V Leiden • Activated Protein C resistance • Protein C deficiency • Protein S Deficiency • Oral contraceptives • Pregnancy Dr. Haug reviews the literature on soccer ballrelated injuries and especially how the relative softness of the ball allows deformation of the ball to impact the globe. The time the soccer ball remains in contact with the globe is longer than other projectiles, and there is a suction effect that can increase the distortion of the ocular anatomy in addition to the usual effects of blunt
Fig. 7. Color fundus photography at 1-day follow-up shows reperfusion of the retinal vasculature.
Fig. 9. Optical coherence tomography with persistent inner retinal thickening and hyperreflectivity.
DIAGNOSTIC AND THERAPEUTIC CHALLENGES
225
traumatic rotation of the globe may also result from concussive head injuries, inducing CRAO. These conditions may cause damage to arterial endothelial cells with exposure to the bloodstream, which stimulates platelet aggregation and thrombus formation. Dr. Haug also states that head trauma can activate the complement cascade, and that Complement Factor 5 leads to neutrophil activation, increased expression of adhesion molecules, emigration of neutrophils and chemotaxis, monocyte activation, and mast cell degranulation, resulting in vascular constriction. The result of this complement-driven response may be arteriolar occlusion. Dr. Haug makes recommendations concerning work-up and management of CRAO. The presenters have provided us with follow-up concerning this patient. Fig. 10. Fundus photography at 2-month follow-up showing resolving cherry red spot and continued perfusion.
ocular trauma. There has been only one soccer-ball– related injury resulting in CRAO, and in this eye, there was direct trauma to the globe. Commotio retinae was seen in addition to the CRAO. But, in the case presented here, there was no direct trauma to the eye. So, how did the CRAO occur in the absence of direct ocular trauma, especially in a patient with no other systemic pathology? Dr. Haug notes that closed-eye head trauma can result in compression of the central retinal artery, induced by hematoma, air in the case of orbital emphysema, or raised pressure from soft tissue swelling. She reviews the possibility that arterial vasospasm or sheering injury from
Fig. 11. Fluorescein angiography shows normal filling times and complete perfusion of vasculature.
Follow-up Subsequently, he was taken to the emergency department for immediate imaging and laboratory work-up, along with neurological consultation; his vital signs were within normal limits. Contrastenhanced magnetic resonance imaging of the brain and orbits, angiogram of the head and neck, and venogram of the head, were unremarkable, specifically, excluding acute infarct, hemorrhage, or carotid artery dissection. Additional work-up included transthoracic echocardiogram with bubble study that was unremarkable, basic laboratory testing (complete blood count and chemistry panel) and investigation for hypercoagulability and for underlying inflammatory process. Systemic and intra-arterial tissue plasminogen activator was deferred because of concern for intracranial hemorrhage after suspected trauma. Ocular massage and regimen with intraocular pressurelowering drops (Brimonidine, Timolol, and Bimatoprost) were initiated while the patient was in the emergency department. Within 12 hours form presentation, the patient began hyperbaric oxygen therapy and daily Aspirin. On the next day, his visual acuity in the left eye had improved to counting fingers vision at 1 foot, with persistent relative afferent pupillary defect and an intraocular pressure of 12 mmHg. Fundus examination showed an unchanged cherry red spot but reperfusion of the retinal vascularization (Figure 7), which was confirmed by fluorescein angiography (Figure 8). Optical coherence tomography revealed persistent inner retinal thickening and hyperreflectivity (Figure 9). Ocular massage and hyperbaric oxygen therapy were continued for another 72 hours, whereas the topical
226
RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2016 VOLUME 36 NUMBER 1
Fig. 12. Optical coherence tomography at the most recent follow-up with retinal thinning.
ocular hypotensives were administered for 2 months. A transesophageal echocardiogram further excluded intracardiac thrombus or a patent foramen ovale. There was no arrhythmia noted on Holter monitoring, and the thorough laboratory work-up was negative or within normal limits including lipid profile, Factor V Leiden, homocysteine, fibrinogen, antinuclear antibody, antineutrophil cytoplasmic antibody, C-reactive protein, erythrocyte sedimentation rate, hemoglobin electrophoresis, Factor VII activity, cardiolipin antibody, lupus anticoagulant, serum protein electrophoresis, antithrombin III, protein C, and protein S. In the course of his outpatient follow-up, the visual acuity in the left eye continued to improve and was 20/ 100 at most recent follow-up, 2 months after the initial presentation. The fundus examination showed a resolving cherry red spot (Figure 10), with complete perfusion of the retinal vascularization (Figure 11) with normal filling times. The latest optical coherence tomography revealed retinal thinning (Figure 12). The patient continues to take a daily Aspirin. We thank Drs. Ryder, Oliveira, Dinkin, D’Amico, and Orlin for this interesting case, and Dr. Haug for her consultation.
5. Umeed S, Shafquat S. Commotio-retinae and central retinal artery occlusion after blunt ocular trauma. Eye (Lond) 2004; 18:333–334. 6. Sorr EM, Goldberg R. Traumatic central retinal artery occlusion with sickle cell trait. Am J Ophthalmol 1975;80: 648–652. 7. Vianna RN. Parafoveal arteriolar obstruction after ocular trauma in a patient with systemic lupus erythematosus. Int Ophthalmol 1999;23:111–114. 8. Nobel MJ, Alvarez EV. Combined occlusion of the central retinal artery and central retinal vein following blunt ocular trauma: a case report. Br J Ophthalmol 1987;71:834–836. 9. Dalma-Weiszhausz J, Meza-de Regil A, Martinez-Jardon S, Oliver-Fernandez K. Retinal vascular occlusion following ocular contusion. Graefes Arch Clin Exp Ophthalmol 2005; 243:406–409. 10. Cumurcu T, Doganay S, Demirel S, Cankaya C. Traumatic optic neuropathy and central retinal artery occlusion following blunt ocular trauma. J Clin Med Res 2011;12:55–57. 11. Hayreh SS, Podhajsky PA, Zimmerman MB. Retinal artery occlusion: associated systemic and ophthalmic abnormalities. Ophthalmology 2009;116:1928–1936. 12. Gaydar V, Ezrachi D, Dratviman-Storobinsky O, et al. Reduction of apoptosis in ischemic retinas of two mouse models using hyperbaric oxygen treatment. Invest Ophthalmol Vis Sci 2011;52:7514–7522. 13. Menzel-Severing J, Siekmann U, Weinberger A, et al. Early hyperbaric oxygen treatment for nonarteritic central retinal artery obstruction. Am J Ophthalmol 2012;153: 454–459.
References 1. Horn EP, McDonald HR, Johnson RN, et al. Soccer ballrelated retinal injuries: a report of 13 cases. Retina 2000;20: 604–609. 2. Capao Filipe JA, Fernandes VL, Barros H, et al. Soccer-related ocular injuries. Arch Ophthalmol 2003;121:687–694. 3. Capao Filipe JA. Soccer (football) ocular injuries: an important eye health problem. Br J Ophthalmol 2004;88: 161–163. 4. Vinger PF, Capao Filipe JA. The mechanism and prevention of soccer eye injuries. Br J Ophthalmol 2004;88:167–168.
RETINAÒ, The Journal of Retinal and Vitreous Diseases, encourages readers to submit Diagnostic and Therapeutic Challenges to [email protected]. Cases for the Diagnostic and Therapeutic Challenges section should include a detailed history of the patient, the diagnosis, the workup, the management, and finally, the question or questions that the submitter wishes to have answered by the consultants.
Edited by H. Richard McDonald
Drs. Steven J. Ryder, Cristiano Oliveira, Marc J. Dinkin, Donald J. D’Amico, Anton Orlin, and Sara J. Haug
T
after a routine soccer ball heading. Although there had been head strikes against the ball during the game, there were no direct contusions to the eye, body collisions, or falls. Presenting visual acuity in the left eye was no light perception, and fundus photography revealed a cherry red spot with vascular attenuation and segmentation of the blood column within the vessels, indicating retrograde perfusion (Figure 2). Optical coherence tomography showed increased hyperreflectivity of the inner retinal layers (Figure 3), and a CRAO was confirmed by fluorescein angiography (Figures 4–6). Sports injuries constitute a large portion of traumatic injuries to eyes, particularly among children and young adults.1,2 In the past, it was believed that injury to the globe is rarely caused by balls larger than 4 inches in diameter given the protective effect of the bony orbit. Therefore soccer, with its larger diameter ball, was less likely to cause significant injury. A number of studies have shown this not to be the case; in fact, soccerrelated eye injuries can result in more severe injury than previously recognized with poor visual outcomes.1–3 One case series of 13 soccer-related ocular injuries found final Snellen visual acuity was 20/200 or worse in a quarter of those studied.1 A series of experiments published in 2004 suggest that the mechanism of ocular injury from soccer balls involves deformation of the ball on impact, which allows a small “knuckle” of the ball to enter the orbit and impact the globe.3,4 The authors also found that the time the soccer ball spends in the orbit is longer than other projectiles and there is a secondary suction effect produced on the orbital contents during rebound of the ball. This suction component increases the distortion of the ocular anatomy, which can lead to more severe injuries.4 There is only one case in the literature describing a CRAO after a soccer ball injury.5 In that case, there was direct trauma to the orbit by the soccer ball, in
his case is submitted by Drs. Steven J. Ryder, Cristiano Oliveira, Marc J. Dinkin, Donald J. D’Amico, and Anton Orlin, of the Department of Ophthalmology, Weill Cornell Medical College, New York, New York; commented by Dr. Sara J. Haug, San Francisco, California. Case Report
An 18-year-old healthy white male presented to our retina clinic within 90 minutes of first noticing visual loss in his left eye while playing soccer, soon after a routine soccer ball heading. Throughout the game, there were prior head strikes against the soccer ball but no head-to-head or body collisions or falls. He denied focal neurologic symptoms, headache, or other visual symptoms. There was a history of previous “multiple” concussions not only from collisions during a soccer game but also in the setting of a motor vehicle accident 3 months before the present incident. His general history was otherwise negative, specifically, no medications or illicit drug use. Visual acuity at presentation was 20/20 in the right eye and no light perception in the left eye, with a marked left relative afferent pupillary defect. Intraocular pressure was 15 mmHg in each eye. Slit-lamp examination was normal in both eyes, with no iritis or periorbital swelling. Dilated funduscopic examination was normal in the right eye (Figure 1) and remarkable for mild optic nerve swelling, retinal vascular attenuation with box-carring, and a macular cherry red spot consistent with a central retinal artery occlusion (CRAO) in the left eye (Figure 2); no arterial embolus was observed. Optical coherence tomography (OCT) of the left eye revealed increased hyperreflectivity of the inner retina with loss of architecture (Figure 3). The fluorescein angiography revealed absent retinal perfusion confirming the central retinal arterial occlusion (Figures 4–6 transit time of 18 seconds, 50 seconds, and 3 minutes 16 seconds, respectively). This case is presented for discussion regarding pathogenesis and management.
Dr. Sara J. Haug (San Francisco, California): Dr. Ryder et al present the case of an 18-year-old man with a history of multiple concussions who suffered complete vision loss while playing soccer 221
222
RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2016 VOLUME 36 NUMBER 1
Fig. 1. Color fundus photography of right eye at initial presentation is unremarkable.
contrast to the case presented here, which did not have direct ocular trauma from the soccer ball before the arterial occlusion. In addition to the CRAO, other signs of trauma including commotio retinae were observed. Despite the direct impact of the soccer ball on the orbit, imaging and laboratory work-up were negative, and the authors concluded the CRAO was likely due to arterial vasospasm. The most common cause for a CRAO is atherosclerotic disease of the internal carotid artery in an elderly patient resulting in embolic occlusion of the artery. However, a number of case reports identify trauma as the etiology behind the arterial obstruction. Often, this can be seen in conjunction with other pathology, such as systemic lupus erythematosus, hemoglobinopathies, or coagulation abnormalities, but systemic pathology
Fig. 2. Color fundus photography of left eye at presentation.
is not noted in all cases of traumatic CRAO.6–11 One proposed mechanism by which trauma can lead to a CRAO in cases of concussion or closed-eye head trauma is compression of the central retinal artery induced either by a hematoma, by air in the case of orbital emphysema or by raised intraorbital pressure from soft tissue swelling, resulting in arterial occlusion. Other postulated theories of traumatic CRAO in concussive head injuries include arterial vasospasm or sheering injury from traumatic rotation of the globe. Common to these conditions is damage to the endothelial cells of the artery with exposure of the subintimal tissue to the bloodstream, which can then stimulate platelet aggregation and thrombus formation.8–10 It has also been proposed that activation of the complement cascade, which can occur in concussive head trauma, can lead to vascular occlusion. Specifically, Complement Factor 5 activation leads to neutrophil activation, increased expression of adhesion molecules, emigration of neutrophils and chemotaxis, monocyte activation, and mast cell degranulation, resulting in vascular constriction. Studies done in a cat model confirm this hypothesis by demonstrating transient occlusion of retinal arterioles induced by intravascular complement activation.7 In the case presented here by Dr. Ryder et al, there was no direct ocular trauma with the soccer ball. However, the patient’s history of multiple concussions may have predisposed the patient to an arterial occlusion due to cumulative vascular damage, even with relatively minor trauma. The impact of the head on the soccer ball may have been enough to induce arterial vasospasm or sheering injury, leading to a CRAO. However, it is also possible that the soccer ball heading has nothing to do with the CRAO experienced by our patient, and this is a nontraumatic CRAO, which has a broad differential diagnosis in a young person. Excluding a traumatic cause, the differential diagnosis in our patient includes cardiac valvular disease, embolic disease, hypertension, and vasculitis. Autoimmune disorders, such as systemic lupus erythematosus, polyarteritis nodosa, and Behcet disease, also predispose a patient to arterial occlusions. Conditions leading to hypercoagulability are also on the differential, such as hyperhomocysteinemia, hyperlipidemia, anticardiolipin antibody, antiphospholipid antibody, antithrombin III mutation, polycythemia, Factor V Leiden, activated Protein C resistance, Protein C or S deficiency, oral contraceptive use, and pregnancy. Carotid artery dissection, stroke, and intracranial hemorrhage must also be considered. Work-up for this patient must include a thorough medical history and contrast-enhanced magnetic resonance imaging of the brain and orbits, magnetic
DIAGNOSTIC AND THERAPEUTIC CHALLENGES
223
Fig. 3. Optical coherence tomography of the left eye at initial presentation revealed increased hyperreflectivity of the inner retina with loss of architecture.
resonance angiogram of the head and neck, and magnetic resonance venogram of the head to evaluate for intracranial hemorrhage, infarct, and carotid dissection. An echocardiogram must be performed to rule out cardiac valvular disease such as an atrial myxoma or endocarditis, and electrocardiogram testing should also be performed to evaluate for cardiac arrhythmia. Laboratory tests for hypercoagulability must be sent and a complete blood count and electrolyte work-up. Management of a CRAO has largely been supportive with very few options to improve outcomes. Treatment options, such as acetazolamide infusion, carbogen inhalation, hemodilution, ocular massage, and paracentesis, as well as vasodilators, such as intravenous glyceryl trinitrate, have not been shown to alter the natural history of a CRAO. More recent evidence suggests that hyperbaric oxygen treatments may improve final visual acuity in some patients.12,13
Animal studies have shown that hyperbaric oxygen treatment initiated immediately after arterial occlusion can reduce retinal neuronal apoptosis.13 A retrospective study by Dr. Menzel-Severing et al compared hyperbaric oxygen treatment in patients with CRAO to patients receiving hemodilution only. They found that patients receiving hyperbaric oxygen treatments had a trend toward better visual outcomes compared with hemodilution alone, but this was not statistically significant and some patients did not respond to any treatment.12 A randomized prospective study is necessary to further evaluate hyperbaric oxygen treatment in cases of retinal artery occlusion.
Fig. 4. Fluorescein angiography at initial presentation revealed absent retinal perfusion at transit time of 18 seconds.
Fig. 5. Fluorescein angiography at initial presentation revealed absent retinal perfusion at transit time of 15 seconds and 3 minutes.
Editor’s Note: Drs. Ryder, Oliveira, Dinkin, D’Amico, and Orlin have presented an 18-year-old male with CRAO after a routine soccer ball heading without direct ocular trauma. The patient is presented for discussion of
224
RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2016 VOLUME 36 NUMBER 1
Fig. 8. Fluorescein angiography at 1-day follow-up illustrating reperfusion of retinal vasculature.
Fig. 6. Fluorescein angiography at initial presentation revealed absent retinal perfusion at transit time of 16 seconds.
pathogenesis and management of CRAO in a patient with multiple previous concussions. Dr. Sara Haug has consulted and provided us with a differential diagnosis of nontraumatic CRAO in a young person. 1. Cardiac • Valvular disease • Embolic disease • Hypertension
2. Autoimmune • Lupus • Polyarteritis nodosa • Bechet’s disease 3. Hypercoagulability • Hyperhomocysteinemia • Hyperlipidemia • Anticardiolipin antibody • Antiphospholipid antibody • Antithrombin III mutation • Polycythemia • Factor V Leiden • Activated Protein C resistance • Protein C deficiency • Protein S Deficiency • Oral contraceptives • Pregnancy Dr. Haug reviews the literature on soccer ballrelated injuries and especially how the relative softness of the ball allows deformation of the ball to impact the globe. The time the soccer ball remains in contact with the globe is longer than other projectiles, and there is a suction effect that can increase the distortion of the ocular anatomy in addition to the usual effects of blunt
Fig. 7. Color fundus photography at 1-day follow-up shows reperfusion of the retinal vasculature.
Fig. 9. Optical coherence tomography with persistent inner retinal thickening and hyperreflectivity.
DIAGNOSTIC AND THERAPEUTIC CHALLENGES
225
traumatic rotation of the globe may also result from concussive head injuries, inducing CRAO. These conditions may cause damage to arterial endothelial cells with exposure to the bloodstream, which stimulates platelet aggregation and thrombus formation. Dr. Haug also states that head trauma can activate the complement cascade, and that Complement Factor 5 leads to neutrophil activation, increased expression of adhesion molecules, emigration of neutrophils and chemotaxis, monocyte activation, and mast cell degranulation, resulting in vascular constriction. The result of this complement-driven response may be arteriolar occlusion. Dr. Haug makes recommendations concerning work-up and management of CRAO. The presenters have provided us with follow-up concerning this patient. Fig. 10. Fundus photography at 2-month follow-up showing resolving cherry red spot and continued perfusion.
ocular trauma. There has been only one soccer-ball– related injury resulting in CRAO, and in this eye, there was direct trauma to the globe. Commotio retinae was seen in addition to the CRAO. But, in the case presented here, there was no direct trauma to the eye. So, how did the CRAO occur in the absence of direct ocular trauma, especially in a patient with no other systemic pathology? Dr. Haug notes that closed-eye head trauma can result in compression of the central retinal artery, induced by hematoma, air in the case of orbital emphysema, or raised pressure from soft tissue swelling. She reviews the possibility that arterial vasospasm or sheering injury from
Fig. 11. Fluorescein angiography shows normal filling times and complete perfusion of vasculature.
Follow-up Subsequently, he was taken to the emergency department for immediate imaging and laboratory work-up, along with neurological consultation; his vital signs were within normal limits. Contrastenhanced magnetic resonance imaging of the brain and orbits, angiogram of the head and neck, and venogram of the head, were unremarkable, specifically, excluding acute infarct, hemorrhage, or carotid artery dissection. Additional work-up included transthoracic echocardiogram with bubble study that was unremarkable, basic laboratory testing (complete blood count and chemistry panel) and investigation for hypercoagulability and for underlying inflammatory process. Systemic and intra-arterial tissue plasminogen activator was deferred because of concern for intracranial hemorrhage after suspected trauma. Ocular massage and regimen with intraocular pressurelowering drops (Brimonidine, Timolol, and Bimatoprost) were initiated while the patient was in the emergency department. Within 12 hours form presentation, the patient began hyperbaric oxygen therapy and daily Aspirin. On the next day, his visual acuity in the left eye had improved to counting fingers vision at 1 foot, with persistent relative afferent pupillary defect and an intraocular pressure of 12 mmHg. Fundus examination showed an unchanged cherry red spot but reperfusion of the retinal vascularization (Figure 7), which was confirmed by fluorescein angiography (Figure 8). Optical coherence tomography revealed persistent inner retinal thickening and hyperreflectivity (Figure 9). Ocular massage and hyperbaric oxygen therapy were continued for another 72 hours, whereas the topical
226
RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2016 VOLUME 36 NUMBER 1
Fig. 12. Optical coherence tomography at the most recent follow-up with retinal thinning.
ocular hypotensives were administered for 2 months. A transesophageal echocardiogram further excluded intracardiac thrombus or a patent foramen ovale. There was no arrhythmia noted on Holter monitoring, and the thorough laboratory work-up was negative or within normal limits including lipid profile, Factor V Leiden, homocysteine, fibrinogen, antinuclear antibody, antineutrophil cytoplasmic antibody, C-reactive protein, erythrocyte sedimentation rate, hemoglobin electrophoresis, Factor VII activity, cardiolipin antibody, lupus anticoagulant, serum protein electrophoresis, antithrombin III, protein C, and protein S. In the course of his outpatient follow-up, the visual acuity in the left eye continued to improve and was 20/ 100 at most recent follow-up, 2 months after the initial presentation. The fundus examination showed a resolving cherry red spot (Figure 10), with complete perfusion of the retinal vascularization (Figure 11) with normal filling times. The latest optical coherence tomography revealed retinal thinning (Figure 12). The patient continues to take a daily Aspirin. We thank Drs. Ryder, Oliveira, Dinkin, D’Amico, and Orlin for this interesting case, and Dr. Haug for her consultation.
5. Umeed S, Shafquat S. Commotio-retinae and central retinal artery occlusion after blunt ocular trauma. Eye (Lond) 2004; 18:333–334. 6. Sorr EM, Goldberg R. Traumatic central retinal artery occlusion with sickle cell trait. Am J Ophthalmol 1975;80: 648–652. 7. Vianna RN. Parafoveal arteriolar obstruction after ocular trauma in a patient with systemic lupus erythematosus. Int Ophthalmol 1999;23:111–114. 8. Nobel MJ, Alvarez EV. Combined occlusion of the central retinal artery and central retinal vein following blunt ocular trauma: a case report. Br J Ophthalmol 1987;71:834–836. 9. Dalma-Weiszhausz J, Meza-de Regil A, Martinez-Jardon S, Oliver-Fernandez K. Retinal vascular occlusion following ocular contusion. Graefes Arch Clin Exp Ophthalmol 2005; 243:406–409. 10. Cumurcu T, Doganay S, Demirel S, Cankaya C. Traumatic optic neuropathy and central retinal artery occlusion following blunt ocular trauma. J Clin Med Res 2011;12:55–57. 11. Hayreh SS, Podhajsky PA, Zimmerman MB. Retinal artery occlusion: associated systemic and ophthalmic abnormalities. Ophthalmology 2009;116:1928–1936. 12. Gaydar V, Ezrachi D, Dratviman-Storobinsky O, et al. Reduction of apoptosis in ischemic retinas of two mouse models using hyperbaric oxygen treatment. Invest Ophthalmol Vis Sci 2011;52:7514–7522. 13. Menzel-Severing J, Siekmann U, Weinberger A, et al. Early hyperbaric oxygen treatment for nonarteritic central retinal artery obstruction. Am J Ophthalmol 2012;153: 454–459.
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RETINAÒ, The Journal of Retinal and Vitreous Diseases, encourages readers to submit Diagnostic and Therapeutic Challenges to [email protected]. Cases for the Diagnostic and Therapeutic Challenges section should include a detailed history of the patient, the diagnosis, the workup, the management, and finally, the question or questions that the submitter wishes to have answered by the consultants.
