Complications Ocular Robert D.
of Glaucoma
Decompression Retinopathy
Fechtner, MD; Donald Minckler, MD; Robert N. Weinreb, MD; George Frangei, MD;
\s=b\ In seven eyes of four patients, retinal hemorrhages were observed following trabeculectomy under both local and gen-
eral anesthesia. The hemorrhages were diffuse, both deep and superficial, and many had white centers when first observed. Two patients were young healthy male myopes undergoing primary trabeculectomy. The third patient was a young man with chronic uveitis. The fourth patient was an elderly man with primary open angle glaucoma who had an acute rise in intraocular pressure following cataract extraction. Intraocular pressure and visual results appeared unaffected by the hemorrhages. Retinal hemorrhages associated with ocular decompression appear to be relatively benign.
(Arch Ophthalmol. 1992;110:965-968) TXTith entry into the anterior chamber ''
during glaucoma filtering
sur¬
gery, there is immediate ocular hypotony. Hemodynamic changes, including suprachoroidal hemorrhage, may de¬ velop, partly due to sudden decompres¬ sion of the eye. We report on seven eyes of four patients who evidenced an un¬ usual pattern of retinal hemorrhage immediately following glaucoma filter¬ ing surgery under both local and gen¬ eral anesthesia. REPORT OF CASES
Case 1.—A first examined
Accepted
Surgery
19-year-old white man was February 6, 1990. Ocular
on
for publication January 28, 1992. From the Department of Ophthalmology, University of California, San Diego (Drs Fechtner and Weinreb); Doheny Eye Institute, Los Angeles, Calif (Drs Minckler and Frangei); and Northwestern University, Chicago, Ill (Dr Jampol). Dr Fechtner is now with the Department of Ophthalmology, University of Louisville, Kentucky. Reprint requests to UCSD/Shiley Eye Center\p=m-\ 0946, 9415 Campus Point Dr, La Jolla, CA 92093\x=req-\ 0946 (Dr Weinreb).
history was significant for intraocular pres¬ sure as high as 38 mm Hg bilaterally in spite
of medical treatment. Treatment at the time of initial examination was 0.5% timolol maleate twice per day, 2% epinephrine hydrochloride twice per day, and 2% pilocarpine hydrochloride four times per day. On initial examination, visual acuity with correction was 20/25 OD (-17.50+1.00x004°) and 20/25 OS (-17.25+0.75x170°). The anterior seg¬ ments appeared normal and typically myopic with wide open angles. The optic nerves exhibited glaucomatous cupping, greatest in the inferotemporal quadrant, worse in the right eye. Automated threshold perimetry demonstrated glauco¬ matous visual field defects consistent with the appearance of the optic nerves. A trabeculectomy was performed on the right eye with the patient under general an¬ esthesia on April 4,1990. On the first postop¬ erative day, retinal hemorrhages were noted in the peripapillary area and peripheral ret¬ ina of the eye that was operated on. No such hemorrhages were noted in the contralateral eye, which was not operated on. Because of intraocular pressures in the range of 40 to 50 mm Hg while not receiving carbonic anhydrase inhibitors, trabeculec¬ tomy was performed on the left eye 5 days later with the patient under general anes¬ thesia. Immediately after surgery, fundus examination revealed blot retinal hemor¬ rhages, some with white centers, in the left eye. These were located in the posterior pole and the periphery. Optic nerve head hemor¬ rhages were also observed (Fig 1). The hem¬ orrhages in the right eye were clearing. Subsequently, the retinal hemorrhages cleared in both eyes over several weeks. Several months postoperatively, intraoc¬ ular pressures were 12 mm Hg in both eyes and visual acuity had returned to preopera¬ tive levels. Case 2.—A 15-year-old Oriental man com¬ plained of poor vision, occasional ocular pain, and photohobia. The referring physician started 0.5% levobunolol hydrochloride ther¬ apy in both eyes twice per day. At initial examination on August 8, 1990, visual acuity with correction was 20/20 OD (-4.50+0.25x150°) and 20/100 OS
Downloaded From: http://archopht.jamanetwork.com/ by a New York University User on 06/03/2015
Lee M.
Jampol,
MD
(-5.00+0.50x150°). Color vision tested by Ishihara plates was reported as 13/15 OD and
3/15 OS. A was
gl'ade 2 afferent pupillary defect
present in the left eye.
Results of external examination were nor¬ 12-mm corneas and brown irides with no transillumination defects. Gonioscopy revealed wide open angles with a flat iris insertion. Intraocular pressures were 63 mm Hg OD and 67 mm Hg OS while receiving treatment with 0.5% levobunolol twice per day. There was extensive glaucomatous cupping, greater in the left eye than the right eye, and arterial pulsations in both eyes. Acetazolamide therapy, 250 mg four times per day, was started. The next day the intraocular pressure was 48 mm Hg OD and 56 mm Hg OS, with no arterial pulsations. Automated threshold perimetry revealed glaucomatous visual field defects consistent with the appearance of the optic nerves. De¬ spite maximal tolerated medications, includ¬ ing levobunolol, pilocarpine, dipivefrin, and acetazolamide, intraocular pressure re¬ mained in the range of 40 to 50 mm Hg. A trabeculectomy was performed in the left eye without complications on August 15, 1990, with the patient under general anes¬ thesia. On the first postoperative day, scat¬ tered blot hemorrhages were observed throughout the retina in the left eye. The contralateral fundus was normal. Due to microcystic corneal edema in the right eye and an intraocular pressure of 60
mal, with clear
mm
Hg, a trabeculectomy was performed on
the right eye 2 weeks later with the patient under local anesthesia. On the first postop¬ erative day, scattered blot retinal hemor¬ rhages were observed in the posterior pole. Many of these hemorrhages appeared to have white centers (Fig 2). There were con¬ fluent deep retinal hemorrhages in the pe¬ riphery, with a preretinal hemorrhage. The hemorrhages in the left eye were resolving, and no new hemorrhages were observed. Ten months postoperatively, intraocular pressure was less than 15 mm Hg OU. Visual acuity had returned to preoperative levels. No hemorrhages were present. Case 3.—A 13-year-old Oriental boy was referred to the glaucoma clinic for help with
1.—Patient 1. Deep retinal hemorrhages are present near the macula, inferior to the optic nerve head and outside the superior vas¬
Fig
cular arcade. The blot hemorrhage below the superior arcade appears to have a white center (arrow). Optic nerve head hemorrhages are
present.
control of intraocular pressure. His history included chronic (idiopathic) anterior and posterior uveitis suggestive of pars planitis in both eyes and secondary glaucoma. Initial symptoms dated to approximately age 10 years. Intraocular pressure had varied be¬ tween the low teens and 40 mm Hg OU. Disc examination on June 22,1990, revealed cupto-disc ratios of about 0.1 in both eyes, asso¬ ciated with disc hyperemia and active in¬ traocular inflammation. The intraocular pressure was 17 mm Hg OD and 30 mm Hg OS. Medical treatment at the time of refer¬ ral included 0.5% timolol maléate twice per day, 1% epinephrine hydrochloride twice per day, 4% pilocarpine hydrochloride four times per day, acetazolamide, 125 mg four times per day, topical atropine intermittently, and topical and systemic steroids. During the course of medical treatment, mild posterior subcapsular lens opacities had developed, and mild cystoid macular edema was present in the left eye. Results of screening tests for uveitis, including a test for Lyme disease and HLA typing, were considered negative or noncontributory. A lumbar puncture did reveal nonspecific elevation of cerebrospinal fluid protein. Results of a magnetic resonance im¬ aging scan were normal. Control of intraocular pressure control became increasingly difficult whether or not the patient was receiving systemic steroid therapy, and rapid deterioration of his optic discs and visual fields had been documented over the previous few months in spite of maximal tolerated medical therapy. On initial examination in the glaucoma clinic on December 21, 1990, visual acuity was 20/30 OU. Intraocular pressure was 19 mm Hg OD and 22 mm Hg OS. Gonioscopy revealed open angles except for scattered mild peripheral anterior synechiae in the left eye and a focal area of peripheral anterior synechiae at 7 o'clock in the right eye. Rubeosis was not noted. Neither eye had anterior
Fig 2.—Patient 2.
Diffuse deep retinal hemorrhages, many with white present in the posterior pole. There is dilation and slight beading or irregularity of the veins. Optic nerve hemorrhages are also present.
centers,
are
chamber cells evident. Snowbanklike accu¬ mulations of debris were noted interiorly along the vitreous base, especially in the left eye. The cup-to-disc ratio was estimated to be 0.6 OD and 0.9 OS. No retinal vasculitis was
apparent.
Intraocular pressure was documented to vary between 11 and 40 mm Hg without clear correlation to inflammation and was usually higher in the left eye. Because of clearly documented deterioration of the discs and the left visual field despite maximal toler¬ ated medical therapy, we elected to perform trabeculectomy on the left eye on January 2, 1991, with the patient under general anes¬ thesia and on the right eye the following day. Surgery was uneventful. On the first postoperative day, peripapillary and peripheral retinal hemorrhages were noted in the left eye. Many of these hemorrhages had white centers (Fig 3). No hemorrhages were present in the right eye at this time. The right eye was examined immediately on completion of surgery, and a similar pat¬ tern of hemorrhages was present (Fig 3). Postoperatively, the right, more normal disc developed marked hyperemia and disc swell¬ ing, virtually obliterating the optic cup. This disc swelling abated over several days. By February 5, 1991, the retinal hemorrhages had cleared in both eyes. The optic nerve cupping appeared increased in both eyes compared with preoperative appearances, although neither visual field had further de¬ teriorated. Despite the use of 5-fluorouracil therapy and removable sutures, intraocular pres¬ sures rose to the mid-20s, and there was marked conjunctival inflammation in both eyes. The filtration blebs gradually flattened and failed. Inflammation recurred in both eyes, and systemic steroid therapy was re¬ sumed. A glaucoma drainage implant was placed in the left eye on April 17,1991. Med¬ ications were required, including 0.5%
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levobunolol hydrochloride twice per day in both eyes, 4% pilocarpine hydrochloride in the right eye, and acetazolamide. As of June 19, 1991, intraocular pressures were 20 mm Hg OD and 18 mm Hg OS. Further inter¬ vention may be necessary depending on the resolution of intraocular inflammation. CASE 4.—An 83-year-old Asian man was known to have primary open angle glaucoma since 1985. At that time, intraocular pressure was 14 mm Hg OU while he was receiving treatment of 0.5%> timolol maléate in both eyes twice per day, 0.1% dipivefrin hydro¬ chloride in both eyes twice per day, 4% pilo¬ carpine hydrochloride in both eyes four times per day, and oral methazolamide, 50 mg twice per day. Cup-to-disc ratio at that time was estimated as 0.4 OD and 0.5 OS. The patient was not compliant and was unavail¬ able for follow-up. In 1989, visual acuity was 20/80 OD and light perception in the left eye, with intraoc¬ ular pressure of 18 mm Hg OD and 24 mm Hg OS. Optic nerve cupping was increased, and the cup-to-disc ratio was judged to be 0.6 OD and 0.9 OS. The poor vision in the left eye was attributed to glaucoma. Medical therapy was resumed, and, in March 1990, the patient un¬ derwent argon laser trabeculoplasty in both eyes. No retinal hemorrhages were observed following the laser procedures. In November 1990 visual acuity was 3/200 OD and no light perception in the left eye, with a dense cataract in the right eye. Intraocular pressure was 14 mm Hg OD and 17 mm Hg OS, with a cup-to-disc ratio of 0.6 OD and 0.99 OS. An extracapsular cataract extraction with posterior chamber intraocular lens implan¬ tation was performed on the right eye in February 1991. Postoperatively, the intraoc¬ ular pressure rose to 40 mm Hg and was not responsive to treatment with timolol, apraclonidine, acetazolamide, and mannitol. Ten days after the cataract surgery, a limbus-based inferotemporal trabeculec-
Fig 3.—Patient 3. Left, Fundus photograph of the left eye 1 day following trabeculectomy, demonstrating peripapillary retinal hemorrhage and deep retinal hemorrhages, many with white centers. Right, Fundus photograph of the right eye 1 day following trabeculectomy, demonstrating a pattern of retinal hemorrhages similar to what occurred in the left eye. tomy was performed with the patient under local anesthesia. Visual acuity following the
trabeculectomy
was
poor, and examination
revealed diffuse deep retinal hemorrhages throughout the fundus, but predominantly within the temporal vascular arcades (Fig 4). A fluorescein angiogram was of poor quality due to cloudy ocular media; it did not reveal any vascular abnormality. Visual acuity had returned to 20/100 OD at the 4-month postoperative visit, with cystoid macular edema noted on fundus examina¬ tion.
COMMENT
We have observed retinal hemor¬
rhages in seven eyes of four patients as a sequela of trabeculectomy. Three pa¬
tients
were
otherwise
men, two Oriental and
healthy young Caucasian,
one
for whom the surgery was a primary trabeculectomy. In all patients the in¬ traocular pressure was relatively high prior to treatment. The fourth patient was an elderly Oriental man whose in¬ traocular pressure was high as a com¬ plication of cataract surgery. Patient 1 had limited peripapillary and peripheral hemorrhages. The reti¬ nal hemorrhages appeared to be deep. A few appeared to have white centers, possibly consisting of fibrin. Patient 2 had blot retinal hemorrhages through¬ out the fundus, several with white cen¬ ters, and a preretinal hemorrhage in the periphery. Patient 3 had peripapillary hemorrhages that appeared superficial and more peripheral deep blot hemor¬ rhages, many with white centers. The pattern in patient 4 included scattered and confluent deep intraretinal hemor¬
rhages.
Retinal hemorrhages following tra¬ beculectomy may be directly related to the sudden lowering of intraocular pres¬ sure. We can postulate several mecha-
nisms
venous
cases
between arterial
by which this may occur. The reported may represent the same or different mechanisms of injury. It is possible that there was some in¬ herited or acquired vascular abnormality in these eyes, resulting in increased cap¬ illary fragility. However, no vascular ab¬
normalities were noted on any of the ex¬ aminations prior to surgery, and there was no history of easy bruising or bleed¬ ing to suggest systemic vascular fra¬ gility. None of the patients was known to be taking aspirin or any other medication that might promote bleeding. Valsalva retinopathy is a well-known entity that is seen following episodes of increased intrathoracic pressure.1 In five of the eyes described, surgery was performed with the patients under gen¬ eral anesthesia. A difficult extubation could theoretically be associated with a Valsalva phenomenon, but there are differences between the cases reported and the typical presentation of Valsalva
retinopathy.
We do not believe these are cases of Valsalva retinopathy for the following reasons: (1) Valsalva retinopathy is usu¬ ally a bilateral event. In these patients only the eye that was operated on had retinal hemorrhages, while the con¬ tralateral eye was unchanged. (2) When the second eye underwent surgery in three patients, that eye had retinal hemorrhages, while the eye that was previously operated on had no further hemorrhages. (3) These hemorrhages occurred with patients under both gen¬ eral and local anesthesia. When the intraocular pressure was lowered surgically, retinal and choroidal blood flow may have been suddenly increased, at least transiently. This could have temporarily overwhelmed the capacitance of the capillary bed and
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system, resulting in a mismatch
perfusion and capil¬ lary capacitance or venous drainage. In other words, the acute lowering of in¬ traocular pressure might have reduced the resistance to blood flow, and the in¬ creased blood flow might have over¬ whelmed the mechanical stability of the capillaries, resulting in multiple focal
endothelial leaks. The presence of a fi¬ brin center in the deep hemorrhages would be consistent with this. A similar pattern has been described in eyes with a central artery occlusion that sponta¬ neously recanalized in patients with sickle cell disease.2 Healthy retinal blood vessels are ca¬ pable of efficient autoregulation. In an¬ imal models, autoregulation maintains blood flow over a wide range of perfu¬ sion and intraocular pressures.3·4 De¬ fects in this autoregulation have been reported in patients with glaucoma and may contribute to the development of the observed hemorrhages.5·6 Another concept that might be in¬ voked to explain the hemorrhages ob¬ served in these cases following sudden decompression of intraocular pressure is to view them as a variation of central retinal vein occlusion. In a relatively young, healthy nerve, such as in patient 3, with a large complement of axons, sudden lowering of intraocular pressure could be expected to induce a forward shift in the lamina cribrosa and acute blockage of axonal transport.7 The rela¬ tively abrupt packing of intraaxonal materials into the disc tissue might in turn compress the central retinal vein and precipitate a hemorrhagic retinop¬ athy resembling vein occlusion. In pa¬ tient 3, the disc in the right eye became markedly swollen (disc swelling), with obliteration of what had been a 0.6
cup-to-disc
ratio. Disc swelling oc¬ curred in the left eye following sur¬ gery but was less obvious because op¬ tic atrophy had been more advanced. Most patients with glaucoma who undergo filtering surgery are older and may have less efficient retinal autoreg¬ ulation. The intraocular pressures in the three young men were relatively high, resulting in a relatively large drop in intraocular pressure and a corre¬ spondingly large presumed increase in arterial perfusion pressure. This large change may have overwhelmed the autoregulatory capacity of the retinal vasculature, resulting in the multiple focal hemorrhages observed. We are unaware of other reports of retinal hemorrhages following trabec¬ ulectomy. Although visual acuity is of¬ ten poor in the immediate postoperative period, reasons such as corneal irregu¬ larity, microhyphema, or choroidal ef¬ fusion are usually identified. Typically, the clinician may not examine the pos¬ terior pole in the first weeks following glaucoma filtering surgery. It is possi¬ ble that cases similar to those reported are undetected. Supraehoroidal hemorrhage follow¬ ing glaucoma surgery in the elderly glaucoma patient is often a devastating event and may occur through a related
mechanism. Unlike retinal blood flow, choroidal blood flow is not believed to be
subject
significant autoregulation. When intraocular pressure is acutely lowered, choroidal blood flow is most likely increased. In an aged patient, it is likely that vascular fragility is present. to
Hence, when the arterial flow to the choroid is increased, the vascular bed
may not be able to handle the increased blood flow, resulting in vascular rup¬ ture and suprachoroidal hemorrhage.*·" Visual results are often poor following suprachoroidal hemorrhage associated with glaucoma filtering surgery, in con¬ trast to the patients described herein with retinal hemorrhages, who have a good visual prognosis. In the two pa¬ tients for whom long-term follow-up was available, visual acuity returned to near preoperative levels, and glaucoma surgery successfully lowered intraocu¬ lar pressure. As has been recommended for glau¬ coma surgery in aged individuals with high intraocular pressure and other risk factors for choroidal hemorrhage, such as aphakia and systemic hypertension, we believe it may be beneficial to lower intraocular pressure as much as possi¬ ble before surgically entering the eye of a young patient. Treatment with os¬ motic agents may be of benefit, al-
though
this remains
speculative. Such
treatment may involve additional
ex¬
pense as well as hazards from side effects and may not be necessary, as the retinal hemorrhages appear benign. It may also be beneficial to prevent postoperative hypotony by suturing the scierai flap tightly and using removable sutures or laser suturolysis to more closely regulate postoperative intraoc¬ ular pressure. We have reported seven eyes of four patients with retinal hemor¬
rhages following glaucoma filtering surgery. These hemorrhages seem to be related to the sudden lowering of
intraocular pressure and may be the result of focal capillary leakage. Fail¬ ure of autoregulation of retinal blood flow may contribute to the develop¬ ment of such hemorrhages. In the two patients for whom long-term follow-up was available, both visual and intraocular pressure results were excellent, and these hemorrhages were a relatively benign event. The filtering surgery failed in the third patient, who had chronic uveitis. In the fourth patient, control of intraoc¬ ular pressure was good, and visual acuity was limited by cystoid macular edema, which may have been related to cataract surgery.
References
hemorrhagic retinopaOphthalmol Soc. 1972;70:298-306. 2. Jampol LM, Condon P, Dizon-Moore R, Serjeant G, Schulman JA. Salmon-patch hemorrhages 1. Duane TD. Valsalva
thy.
Trans Am
after central retinal artery occlusion in sickle cell disease. Arch Ophthalmol. 1981;99:237-240. 3. Geijer C, Bill A. Effects of raised intraocular pressure on retinal, prelaminar, laminar, and retrolaminar optic nerve blood flow in monkeys. Invest Ophthalmol Vis Sci. 1979;18:1030-1042. 4. Sossi N, Anderson DR. Effect of elevated in-
traocular pressure on blood flow: occurrence in the
optic nerve head studied with iodoantipyrine I 125. Arch Ophthalmol. 1983;101:98-101. 5. Grunwald JE, Riva CE, Stone RA, Keates EU, Petrig BL. Retinal autoregulation in open\x=req-\ angle glaucoma. Ophthalmology. 1984;91:1690\x=req-\ cat
1694. 6. Sponsel WE, DePaul KL, Kaufman PL. Correlation of visual function and retinal leukocyte velocity in glaucoma. Am J Ophthalmol. 1990;109: 49-54.
Downloaded From: http://archopht.jamanetwork.com/ by a New York University User on 06/03/2015
7. Minckler DS, Bunt AH. Axoplasmic transport in ocular hypotomy and papilledema in the monkey. Arch Ophthalmol. 1977;95:1430-1436. 8. Cantor LB, Katz LJ, Spaeth GL. Complications of surgery in glaucoma: suprachoroidal ex-
pulsive hemorrhage in glaucoma patients undergoing intraocular surgery. Ophthalmology. 1985;92:
1266-1270. 9. Givens K, Shields MB. Suprachoroidal hemorrhage after glaucoma filtering surgery. Am J
Ophthalmol. 1987;103:689-694.
of Glaucoma
Decompression Retinopathy
Fechtner, MD; Donald Minckler, MD; Robert N. Weinreb, MD; George Frangei, MD;
\s=b\ In seven eyes of four patients, retinal hemorrhages were observed following trabeculectomy under both local and gen-
eral anesthesia. The hemorrhages were diffuse, both deep and superficial, and many had white centers when first observed. Two patients were young healthy male myopes undergoing primary trabeculectomy. The third patient was a young man with chronic uveitis. The fourth patient was an elderly man with primary open angle glaucoma who had an acute rise in intraocular pressure following cataract extraction. Intraocular pressure and visual results appeared unaffected by the hemorrhages. Retinal hemorrhages associated with ocular decompression appear to be relatively benign.
(Arch Ophthalmol. 1992;110:965-968) TXTith entry into the anterior chamber ''
during glaucoma filtering
sur¬
gery, there is immediate ocular hypotony. Hemodynamic changes, including suprachoroidal hemorrhage, may de¬ velop, partly due to sudden decompres¬ sion of the eye. We report on seven eyes of four patients who evidenced an un¬ usual pattern of retinal hemorrhage immediately following glaucoma filter¬ ing surgery under both local and gen¬ eral anesthesia. REPORT OF CASES
Case 1.—A first examined
Accepted
Surgery
19-year-old white man was February 6, 1990. Ocular
on
for publication January 28, 1992. From the Department of Ophthalmology, University of California, San Diego (Drs Fechtner and Weinreb); Doheny Eye Institute, Los Angeles, Calif (Drs Minckler and Frangei); and Northwestern University, Chicago, Ill (Dr Jampol). Dr Fechtner is now with the Department of Ophthalmology, University of Louisville, Kentucky. Reprint requests to UCSD/Shiley Eye Center\p=m-\ 0946, 9415 Campus Point Dr, La Jolla, CA 92093\x=req-\ 0946 (Dr Weinreb).
history was significant for intraocular pres¬ sure as high as 38 mm Hg bilaterally in spite
of medical treatment. Treatment at the time of initial examination was 0.5% timolol maleate twice per day, 2% epinephrine hydrochloride twice per day, and 2% pilocarpine hydrochloride four times per day. On initial examination, visual acuity with correction was 20/25 OD (-17.50+1.00x004°) and 20/25 OS (-17.25+0.75x170°). The anterior seg¬ ments appeared normal and typically myopic with wide open angles. The optic nerves exhibited glaucomatous cupping, greatest in the inferotemporal quadrant, worse in the right eye. Automated threshold perimetry demonstrated glauco¬ matous visual field defects consistent with the appearance of the optic nerves. A trabeculectomy was performed on the right eye with the patient under general an¬ esthesia on April 4,1990. On the first postop¬ erative day, retinal hemorrhages were noted in the peripapillary area and peripheral ret¬ ina of the eye that was operated on. No such hemorrhages were noted in the contralateral eye, which was not operated on. Because of intraocular pressures in the range of 40 to 50 mm Hg while not receiving carbonic anhydrase inhibitors, trabeculec¬ tomy was performed on the left eye 5 days later with the patient under general anes¬ thesia. Immediately after surgery, fundus examination revealed blot retinal hemor¬ rhages, some with white centers, in the left eye. These were located in the posterior pole and the periphery. Optic nerve head hemor¬ rhages were also observed (Fig 1). The hem¬ orrhages in the right eye were clearing. Subsequently, the retinal hemorrhages cleared in both eyes over several weeks. Several months postoperatively, intraoc¬ ular pressures were 12 mm Hg in both eyes and visual acuity had returned to preopera¬ tive levels. Case 2.—A 15-year-old Oriental man com¬ plained of poor vision, occasional ocular pain, and photohobia. The referring physician started 0.5% levobunolol hydrochloride ther¬ apy in both eyes twice per day. At initial examination on August 8, 1990, visual acuity with correction was 20/20 OD (-4.50+0.25x150°) and 20/100 OS
Downloaded From: http://archopht.jamanetwork.com/ by a New York University User on 06/03/2015
Lee M.
Jampol,
MD
(-5.00+0.50x150°). Color vision tested by Ishihara plates was reported as 13/15 OD and
3/15 OS. A was
gl'ade 2 afferent pupillary defect
present in the left eye.
Results of external examination were nor¬ 12-mm corneas and brown irides with no transillumination defects. Gonioscopy revealed wide open angles with a flat iris insertion. Intraocular pressures were 63 mm Hg OD and 67 mm Hg OS while receiving treatment with 0.5% levobunolol twice per day. There was extensive glaucomatous cupping, greater in the left eye than the right eye, and arterial pulsations in both eyes. Acetazolamide therapy, 250 mg four times per day, was started. The next day the intraocular pressure was 48 mm Hg OD and 56 mm Hg OS, with no arterial pulsations. Automated threshold perimetry revealed glaucomatous visual field defects consistent with the appearance of the optic nerves. De¬ spite maximal tolerated medications, includ¬ ing levobunolol, pilocarpine, dipivefrin, and acetazolamide, intraocular pressure re¬ mained in the range of 40 to 50 mm Hg. A trabeculectomy was performed in the left eye without complications on August 15, 1990, with the patient under general anes¬ thesia. On the first postoperative day, scat¬ tered blot hemorrhages were observed throughout the retina in the left eye. The contralateral fundus was normal. Due to microcystic corneal edema in the right eye and an intraocular pressure of 60
mal, with clear
mm
Hg, a trabeculectomy was performed on
the right eye 2 weeks later with the patient under local anesthesia. On the first postop¬ erative day, scattered blot retinal hemor¬ rhages were observed in the posterior pole. Many of these hemorrhages appeared to have white centers (Fig 2). There were con¬ fluent deep retinal hemorrhages in the pe¬ riphery, with a preretinal hemorrhage. The hemorrhages in the left eye were resolving, and no new hemorrhages were observed. Ten months postoperatively, intraocular pressure was less than 15 mm Hg OU. Visual acuity had returned to preoperative levels. No hemorrhages were present. Case 3.—A 13-year-old Oriental boy was referred to the glaucoma clinic for help with
1.—Patient 1. Deep retinal hemorrhages are present near the macula, inferior to the optic nerve head and outside the superior vas¬
Fig
cular arcade. The blot hemorrhage below the superior arcade appears to have a white center (arrow). Optic nerve head hemorrhages are
present.
control of intraocular pressure. His history included chronic (idiopathic) anterior and posterior uveitis suggestive of pars planitis in both eyes and secondary glaucoma. Initial symptoms dated to approximately age 10 years. Intraocular pressure had varied be¬ tween the low teens and 40 mm Hg OU. Disc examination on June 22,1990, revealed cupto-disc ratios of about 0.1 in both eyes, asso¬ ciated with disc hyperemia and active in¬ traocular inflammation. The intraocular pressure was 17 mm Hg OD and 30 mm Hg OS. Medical treatment at the time of refer¬ ral included 0.5% timolol maléate twice per day, 1% epinephrine hydrochloride twice per day, 4% pilocarpine hydrochloride four times per day, acetazolamide, 125 mg four times per day, topical atropine intermittently, and topical and systemic steroids. During the course of medical treatment, mild posterior subcapsular lens opacities had developed, and mild cystoid macular edema was present in the left eye. Results of screening tests for uveitis, including a test for Lyme disease and HLA typing, were considered negative or noncontributory. A lumbar puncture did reveal nonspecific elevation of cerebrospinal fluid protein. Results of a magnetic resonance im¬ aging scan were normal. Control of intraocular pressure control became increasingly difficult whether or not the patient was receiving systemic steroid therapy, and rapid deterioration of his optic discs and visual fields had been documented over the previous few months in spite of maximal tolerated medical therapy. On initial examination in the glaucoma clinic on December 21, 1990, visual acuity was 20/30 OU. Intraocular pressure was 19 mm Hg OD and 22 mm Hg OS. Gonioscopy revealed open angles except for scattered mild peripheral anterior synechiae in the left eye and a focal area of peripheral anterior synechiae at 7 o'clock in the right eye. Rubeosis was not noted. Neither eye had anterior
Fig 2.—Patient 2.
Diffuse deep retinal hemorrhages, many with white present in the posterior pole. There is dilation and slight beading or irregularity of the veins. Optic nerve hemorrhages are also present.
centers,
are
chamber cells evident. Snowbanklike accu¬ mulations of debris were noted interiorly along the vitreous base, especially in the left eye. The cup-to-disc ratio was estimated to be 0.6 OD and 0.9 OS. No retinal vasculitis was
apparent.
Intraocular pressure was documented to vary between 11 and 40 mm Hg without clear correlation to inflammation and was usually higher in the left eye. Because of clearly documented deterioration of the discs and the left visual field despite maximal toler¬ ated medical therapy, we elected to perform trabeculectomy on the left eye on January 2, 1991, with the patient under general anes¬ thesia and on the right eye the following day. Surgery was uneventful. On the first postoperative day, peripapillary and peripheral retinal hemorrhages were noted in the left eye. Many of these hemorrhages had white centers (Fig 3). No hemorrhages were present in the right eye at this time. The right eye was examined immediately on completion of surgery, and a similar pat¬ tern of hemorrhages was present (Fig 3). Postoperatively, the right, more normal disc developed marked hyperemia and disc swell¬ ing, virtually obliterating the optic cup. This disc swelling abated over several days. By February 5, 1991, the retinal hemorrhages had cleared in both eyes. The optic nerve cupping appeared increased in both eyes compared with preoperative appearances, although neither visual field had further de¬ teriorated. Despite the use of 5-fluorouracil therapy and removable sutures, intraocular pres¬ sures rose to the mid-20s, and there was marked conjunctival inflammation in both eyes. The filtration blebs gradually flattened and failed. Inflammation recurred in both eyes, and systemic steroid therapy was re¬ sumed. A glaucoma drainage implant was placed in the left eye on April 17,1991. Med¬ ications were required, including 0.5%
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levobunolol hydrochloride twice per day in both eyes, 4% pilocarpine hydrochloride in the right eye, and acetazolamide. As of June 19, 1991, intraocular pressures were 20 mm Hg OD and 18 mm Hg OS. Further inter¬ vention may be necessary depending on the resolution of intraocular inflammation. CASE 4.—An 83-year-old Asian man was known to have primary open angle glaucoma since 1985. At that time, intraocular pressure was 14 mm Hg OU while he was receiving treatment of 0.5%> timolol maléate in both eyes twice per day, 0.1% dipivefrin hydro¬ chloride in both eyes twice per day, 4% pilo¬ carpine hydrochloride in both eyes four times per day, and oral methazolamide, 50 mg twice per day. Cup-to-disc ratio at that time was estimated as 0.4 OD and 0.5 OS. The patient was not compliant and was unavail¬ able for follow-up. In 1989, visual acuity was 20/80 OD and light perception in the left eye, with intraoc¬ ular pressure of 18 mm Hg OD and 24 mm Hg OS. Optic nerve cupping was increased, and the cup-to-disc ratio was judged to be 0.6 OD and 0.9 OS. The poor vision in the left eye was attributed to glaucoma. Medical therapy was resumed, and, in March 1990, the patient un¬ derwent argon laser trabeculoplasty in both eyes. No retinal hemorrhages were observed following the laser procedures. In November 1990 visual acuity was 3/200 OD and no light perception in the left eye, with a dense cataract in the right eye. Intraocular pressure was 14 mm Hg OD and 17 mm Hg OS, with a cup-to-disc ratio of 0.6 OD and 0.99 OS. An extracapsular cataract extraction with posterior chamber intraocular lens implan¬ tation was performed on the right eye in February 1991. Postoperatively, the intraoc¬ ular pressure rose to 40 mm Hg and was not responsive to treatment with timolol, apraclonidine, acetazolamide, and mannitol. Ten days after the cataract surgery, a limbus-based inferotemporal trabeculec-
Fig 3.—Patient 3. Left, Fundus photograph of the left eye 1 day following trabeculectomy, demonstrating peripapillary retinal hemorrhage and deep retinal hemorrhages, many with white centers. Right, Fundus photograph of the right eye 1 day following trabeculectomy, demonstrating a pattern of retinal hemorrhages similar to what occurred in the left eye. tomy was performed with the patient under local anesthesia. Visual acuity following the
trabeculectomy
was
poor, and examination
revealed diffuse deep retinal hemorrhages throughout the fundus, but predominantly within the temporal vascular arcades (Fig 4). A fluorescein angiogram was of poor quality due to cloudy ocular media; it did not reveal any vascular abnormality. Visual acuity had returned to 20/100 OD at the 4-month postoperative visit, with cystoid macular edema noted on fundus examina¬ tion.
COMMENT
We have observed retinal hemor¬
rhages in seven eyes of four patients as a sequela of trabeculectomy. Three pa¬
tients
were
otherwise
men, two Oriental and
healthy young Caucasian,
one
for whom the surgery was a primary trabeculectomy. In all patients the in¬ traocular pressure was relatively high prior to treatment. The fourth patient was an elderly Oriental man whose in¬ traocular pressure was high as a com¬ plication of cataract surgery. Patient 1 had limited peripapillary and peripheral hemorrhages. The reti¬ nal hemorrhages appeared to be deep. A few appeared to have white centers, possibly consisting of fibrin. Patient 2 had blot retinal hemorrhages through¬ out the fundus, several with white cen¬ ters, and a preretinal hemorrhage in the periphery. Patient 3 had peripapillary hemorrhages that appeared superficial and more peripheral deep blot hemor¬ rhages, many with white centers. The pattern in patient 4 included scattered and confluent deep intraretinal hemor¬
rhages.
Retinal hemorrhages following tra¬ beculectomy may be directly related to the sudden lowering of intraocular pres¬ sure. We can postulate several mecha-
nisms
venous
cases
between arterial
by which this may occur. The reported may represent the same or different mechanisms of injury. It is possible that there was some in¬ herited or acquired vascular abnormality in these eyes, resulting in increased cap¬ illary fragility. However, no vascular ab¬
normalities were noted on any of the ex¬ aminations prior to surgery, and there was no history of easy bruising or bleed¬ ing to suggest systemic vascular fra¬ gility. None of the patients was known to be taking aspirin or any other medication that might promote bleeding. Valsalva retinopathy is a well-known entity that is seen following episodes of increased intrathoracic pressure.1 In five of the eyes described, surgery was performed with the patients under gen¬ eral anesthesia. A difficult extubation could theoretically be associated with a Valsalva phenomenon, but there are differences between the cases reported and the typical presentation of Valsalva
retinopathy.
We do not believe these are cases of Valsalva retinopathy for the following reasons: (1) Valsalva retinopathy is usu¬ ally a bilateral event. In these patients only the eye that was operated on had retinal hemorrhages, while the con¬ tralateral eye was unchanged. (2) When the second eye underwent surgery in three patients, that eye had retinal hemorrhages, while the eye that was previously operated on had no further hemorrhages. (3) These hemorrhages occurred with patients under both gen¬ eral and local anesthesia. When the intraocular pressure was lowered surgically, retinal and choroidal blood flow may have been suddenly increased, at least transiently. This could have temporarily overwhelmed the capacitance of the capillary bed and
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system, resulting in a mismatch
perfusion and capil¬ lary capacitance or venous drainage. In other words, the acute lowering of in¬ traocular pressure might have reduced the resistance to blood flow, and the in¬ creased blood flow might have over¬ whelmed the mechanical stability of the capillaries, resulting in multiple focal
endothelial leaks. The presence of a fi¬ brin center in the deep hemorrhages would be consistent with this. A similar pattern has been described in eyes with a central artery occlusion that sponta¬ neously recanalized in patients with sickle cell disease.2 Healthy retinal blood vessels are ca¬ pable of efficient autoregulation. In an¬ imal models, autoregulation maintains blood flow over a wide range of perfu¬ sion and intraocular pressures.3·4 De¬ fects in this autoregulation have been reported in patients with glaucoma and may contribute to the development of the observed hemorrhages.5·6 Another concept that might be in¬ voked to explain the hemorrhages ob¬ served in these cases following sudden decompression of intraocular pressure is to view them as a variation of central retinal vein occlusion. In a relatively young, healthy nerve, such as in patient 3, with a large complement of axons, sudden lowering of intraocular pressure could be expected to induce a forward shift in the lamina cribrosa and acute blockage of axonal transport.7 The rela¬ tively abrupt packing of intraaxonal materials into the disc tissue might in turn compress the central retinal vein and precipitate a hemorrhagic retinop¬ athy resembling vein occlusion. In pa¬ tient 3, the disc in the right eye became markedly swollen (disc swelling), with obliteration of what had been a 0.6
cup-to-disc
ratio. Disc swelling oc¬ curred in the left eye following sur¬ gery but was less obvious because op¬ tic atrophy had been more advanced. Most patients with glaucoma who undergo filtering surgery are older and may have less efficient retinal autoreg¬ ulation. The intraocular pressures in the three young men were relatively high, resulting in a relatively large drop in intraocular pressure and a corre¬ spondingly large presumed increase in arterial perfusion pressure. This large change may have overwhelmed the autoregulatory capacity of the retinal vasculature, resulting in the multiple focal hemorrhages observed. We are unaware of other reports of retinal hemorrhages following trabec¬ ulectomy. Although visual acuity is of¬ ten poor in the immediate postoperative period, reasons such as corneal irregu¬ larity, microhyphema, or choroidal ef¬ fusion are usually identified. Typically, the clinician may not examine the pos¬ terior pole in the first weeks following glaucoma filtering surgery. It is possi¬ ble that cases similar to those reported are undetected. Supraehoroidal hemorrhage follow¬ ing glaucoma surgery in the elderly glaucoma patient is often a devastating event and may occur through a related
mechanism. Unlike retinal blood flow, choroidal blood flow is not believed to be
subject
significant autoregulation. When intraocular pressure is acutely lowered, choroidal blood flow is most likely increased. In an aged patient, it is likely that vascular fragility is present. to
Hence, when the arterial flow to the choroid is increased, the vascular bed
may not be able to handle the increased blood flow, resulting in vascular rup¬ ture and suprachoroidal hemorrhage.*·" Visual results are often poor following suprachoroidal hemorrhage associated with glaucoma filtering surgery, in con¬ trast to the patients described herein with retinal hemorrhages, who have a good visual prognosis. In the two pa¬ tients for whom long-term follow-up was available, visual acuity returned to near preoperative levels, and glaucoma surgery successfully lowered intraocu¬ lar pressure. As has been recommended for glau¬ coma surgery in aged individuals with high intraocular pressure and other risk factors for choroidal hemorrhage, such as aphakia and systemic hypertension, we believe it may be beneficial to lower intraocular pressure as much as possi¬ ble before surgically entering the eye of a young patient. Treatment with os¬ motic agents may be of benefit, al-
though
this remains
speculative. Such
treatment may involve additional
ex¬
pense as well as hazards from side effects and may not be necessary, as the retinal hemorrhages appear benign. It may also be beneficial to prevent postoperative hypotony by suturing the scierai flap tightly and using removable sutures or laser suturolysis to more closely regulate postoperative intraoc¬ ular pressure. We have reported seven eyes of four patients with retinal hemor¬
rhages following glaucoma filtering surgery. These hemorrhages seem to be related to the sudden lowering of
intraocular pressure and may be the result of focal capillary leakage. Fail¬ ure of autoregulation of retinal blood flow may contribute to the develop¬ ment of such hemorrhages. In the two patients for whom long-term follow-up was available, both visual and intraocular pressure results were excellent, and these hemorrhages were a relatively benign event. The filtering surgery failed in the third patient, who had chronic uveitis. In the fourth patient, control of intraoc¬ ular pressure was good, and visual acuity was limited by cystoid macular edema, which may have been related to cataract surgery.
References
hemorrhagic retinopaOphthalmol Soc. 1972;70:298-306. 2. Jampol LM, Condon P, Dizon-Moore R, Serjeant G, Schulman JA. Salmon-patch hemorrhages 1. Duane TD. Valsalva
thy.
Trans Am
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optic nerve head studied with iodoantipyrine I 125. Arch Ophthalmol. 1983;101:98-101. 5. Grunwald JE, Riva CE, Stone RA, Keates EU, Petrig BL. Retinal autoregulation in open\x=req-\ angle glaucoma. Ophthalmology. 1984;91:1690\x=req-\ cat
1694. 6. Sponsel WE, DePaul KL, Kaufman PL. Correlation of visual function and retinal leukocyte velocity in glaucoma. Am J Ophthalmol. 1990;109: 49-54.
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