Cobalt-Chromium Metallosis With Normal Electroretinogram

Ocular cobalt toxicity is a rare phenomenon reported with increased frequency due to the rise of cobalt-chromium metal hip implants. We report the case of a 66-year-old previously healthy man who developed decreased vision due to cobalt-chromium toxicity from a metal-on-metal hip arthroplasty. Our objective was to determine whether the origin of his visual loss was due to toxicity of the optic nerve, of the retina, or of both.; Ocular examination, 10-2 SITA-Standard Humphrey Visual Field (VF), standard full-field electroretinogram (ERG) as indicated by the International Society for Clinical Electrophysiology of Vision (ISCEV), multifocal electroretinogram (mfERG), multifocal visual evoked potentials (mfVEP), and optical coherence tomography (OCT) were conducted.; Ocular examination revealed decreased visual acuity, poor color vision, normal funduscopy, and cecocentral scotomas on VF testing. Because his right eye was amblyopic since childhood, test results from only the left eye are shown. Electrophysiology studies revealed an ISCEV standard full-field ERG with photopic and scotopic responses within normal limits, mfERG with amplitudes and latencies within normal limits, and mfVEP with latencies within normal limits, but with decreased central amplitudes. Peripapillary and macular OCT showed retinal nerve fiber layer and retinal ganglion cell-inner plexiform layer thickness within normal limits.; Because decreased color vision and cecocentral scotoma on 10-2 VF are most consistent with toxic optic neuropathy, and decreased central amplitudes on mfVEP are suggestive of neural dysfunction, we hypothesize that our patient presented with an early stage of optic nerve toxicity that was not yet apparent as a structural abnormality on OCT.

Original Contribution Cobalt-Chromium Metallosis With Normal Electroretinogram Lola M. Grillo, BA, Huy V. Nguyen, MD, Stephen H. Tsang, MD, PhD, Donald C. Hood, PhD, Jeffrey G. Odel, MD Background: Ocular cobalt toxicity is a rare phenomenon reported with increased frequency due to the rise of cobalt- chromium metal hip implants. We report the case of a 66year-old previously healthy man who developed decreased vision due to cobalt-chromium toxicity from a metal-onmetal hip arthroplasty. Our objective was to determine whether the origin of his visual loss was due to toxicity of the optic nerve, of the retina, or of both. Methods: Ocular examination, 10-2 SITA-Standard Humphrey Visual Field (VF), standard full-field electroretinogram (ERG) as indicated by the International Society for Clinical Electrophysiology of Vision (ISCEV), multifocal electroretinogram (mfERG), multifocal visual evoked potentials (mfVEP), and optical coherence tomography (OCT) were conducted. Results: Ocular examination revealed decreased visual acuity, poor color vision, normal funduscopy, and cecocentral scotomas on VF testing. Because his right eye was amblyopic since childhood, test results from only the left eye are shown. Electrophysiology studies revealed an ISCEV standard full-field ERG with photopic and scotopic responses within normal limits, mfERG with amplitudes and latencies within normal limits, and mfVEP with latencies within normal limits, but with decreased central amplitudes. Peripapillary and macular OCT showed retinal nerve fiber College of Physicians and Surgeons (LG, HVN), Columbia University, New York, New York; Department of Ophthalmology (SHT, DCH, JGO), Columbia University, New York, New York; Department of Pathology and Cell Biology (SHT), Institute of Human Nutrition, and Irving Comprehensive Cancer Center, Columbia University, New York, New York; and Department of Psychology (DCH), Columbia University, New York, New York. Supported by NIH grant RO1-EY-02115, R01EY018213, R21AG050437, Core grants 5P30CA013696 and 5P30EY019007; and unrestricted funds from Research to Prevent Blindness, Columbia University, New York, and an equipment grant from Topcon. D. C. Hood reported support of equipment and a grant from Topcon, Inc. and equipment from Heidelberg Engineering. The remaining authors report no conflicts of interest. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the full text and PDF versions of this article on the journal's Web site (www. jneuro-ophthalmology.com). Address correspondence to Jeffrey G. Odel, MD, Edward S. Harkness Institute, 635 W 165th Street, New York, NY 10032; E-mail: [e-mail] Grillo et al: J Neuro-Ophthalmol 2016; 36: 383-388 layer and retinal ganglion cell-inner plexiform layer thickness within normal limits. Conclusion: Because decreased color vision and cecocentral scotoma on 10-2 VF are most consistent with toxic optic neuropathy, and decreased central amplitudes on mfVEP are suggestive of neural dysfunction, we hypothesize that our patient presented with an early stage of optic nerve toxicity that was not yet apparent as a structural abnormality on OCT. Journal of Neuro-Ophthalmology 2016;36:383-388 doi: 10.1097/WNO.0000000000000400 © 2016 by North American Neuro-Ophthalmology Society T he mechanism of visual loss due to a failed cobalt- chromium hip implant remains obscure. Cobalt and chromium ions leak into the bloodstream and surrounding tissues, resulting in markedly elevated serum levels, particularly in cases where retained ceramic debris from a previous ceramic hip transplant grinds down the metallic implant (1-9). Typically within 2 years, these patients develop visual loss, sensory-neural hearing loss, hypothyroidism, and cardiomyopathy (1-9). Reported findings in patients with cobalt toxicity include optic atrophy, impaired choroidal perfusion, abnormal macular function, delays on visual evoked potentials (VEPs), hyperintensities of the anterior visual pathway on magnetic resonance imaging, chorioretinal degeneration, hypofluorescent lesions on indocyanine green chorioangiography, and abnormal electroretinograms (ERGs) (1-13). Few patients have been studied with a combination of electrophysiology, optical coherence tomography (OCT), and visual fields (VFs). We recently evaluated a patient early in the course of visual loss at the time of replacement of a failed cobalt-chromium implant. CASE REPORT A 66-year-old man with a history of childhood amblyopia on his right eye underwent a left total hip arthroplasty with 383 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 1. Cecocentral visual field depression is present in the left eye (Humphrey 10-2). ceramic-on-ceramic pairing. Three years later, the ceramic implant fractured and was replaced with a metal-on-metal implant with a cobalt-chromium femoral head (Zimmer, Warsaw, IN). Nine months later, the patient noted that red traffic lights appeared orange. He began to have difficulty seeing at distance and near, and difficulty hearing, requiring hearing aids for normal conversation. He also noted increasing abdominal distention and ankle swelling, left hip pain, pale diarrhea, a rash, incoordination, and subjective loss of mental clarity. One year after replacement of the femoral head implant, the patient's vision was 20/80, right eye, and 20/30, left eye. He was unable to identify any of the AO-HRR color plates, although pupillary reactions and funduscopy were normal. VF testing in the left eye showed cecocentral depression (Fig. 1). A battery of visual tests were performed. Results are shown only for the left eye because results from the right eye were inconclusive due to amblyopia. Spectral domain OCT revealed normal thickness of the retinal nerve fiber layer (RNFL) and retinal ganglion cell-inner plexiform layer (RGCIPL) (see Supplemental Digital Content, Figure E1, http:// links.lww.com/WNO/A199). Full-field ERG demonstrated normal scotopic and photopic responses (see Supplemental Digital Content, Figure E2, http://links.lww.com/WNO/ A200), and multifocal electroretinographic (mfERG) amplitudes and latencies within normal limits (see Supplemental Digital Content, Figure E3, http://links.lww.com/WNO/ A201). The multifocal visual evoked potential (mfVEP) showed central depression of amplitudes in the left eye (Fig. 2), which corresponded to the cecocentral depression detected on VF testing. The patient's symptoms and examination findings raised concern for cobalt toxicity. A serum cobalt level yielded a concentration of 1,078 mg/L (normal ,0.3 mg/L). The patient underwent revision of the left hip prosthesis. At surgery, ceramic fragments were found in the joint, the FIG. 2. The multifocal VEP responses centrally (A) are significantly smaller than normal (B, red boxes) consistent with depressed central visual field sensitivity (C, red area). OS, left eye; VEP, visual evoked potential. 384 Grillo et al: J Neuro-Ophthalmol 2016; 36: 383-388 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Grillo et al: J Neuro-Ophthalmol 2016; 36: 383-388 Report Type of Exposure Time to Symptom Onset in months 73 g cobalt chloride over 3-yr Unknown period: treatment for pancytopenia and hypercellular bone marrow Meecham and Industrial raw cobalt powder 13 Humphrey exposure for 20 mo (11) working 50 h/wk Steens et al (1) Metal-on-ceramic hip 24 arthroplasty Licht et al (10) 5 Tower (9) Metal-on-metal hip arthroplasty (ASR system, DePuy*) 11 Bhardwaj et al (12) Oral ingestion of two 9 cm cattle magnets (5%-38% cobalt) Unknown Current case Metal-on-metal hip arthroplasty (Zimmer) 9 Symptoms, Examination Findings, and Ancillary Tests Ocular Abnormalities Visual Tests Undocumented Nausea/vomiting, cardiomyopathy Optic nerve atrophy OU; impaired choroidal perfusion Abnormal VF OD; abnormal fluorescein angiography Blood: 234; urine (24-hr collection): 119 Serum: 398 Tinnitus, deafness, vertigo, decreased VA Optic nerve atrophy with temporal pallor OU Delays on VEP OU: improved with decline in serum cobalt Clinical examination only Sight and hearing impairment, numbness of feet, dermatitis Visual and hearing loss, Blood: 549; hypothyroidism; EMG: plasma: 90; mild lower limb amplitude CSF: 11.4; urine reduction; 3 mo later- (24-hr wheelchair bound due to collection): lower limb weakness 1,187 Serum: 122; CSF: Dermatitis, hip pain, anxiety, headache, 2.2; joint fluid: tinnitus, hearing loss, 3,200 incoordination Blood: 112.4; urine Decreased color vision and VA, generalized malaise, (24-hr hypothyroidism, collection): tachycardia, polycythemia 473.2 Serum: 1,078 Decreased color vision and VA, hearing loss, hypothyroidism, ataxia, dermatitis, cognitive decline Optic nerve atrophy and macular malfunction OU Optic nerve, tract, and/or VEP: irregular cortical visual responses; MRI of brain visual cortex with hyperintensity of dysfunction, OU (fundus optic nerves and tracts examination not described) Optic nerve atrophy OU Clinical examination only Optic nerve atrophy OU; bilateral RPE dysfunction Delays on VEP OU; abnormal VF OU; abnormal EOG OU Optic nerve dysfunction OS Normal ERG, mfERG, OCT; mfVEP with decreased central amplitude OS Original Contribution Metal-on-ceramic hip Rizzetti et al arthroplasty (3); Pazzaglia et al (4) Highest Measured Co Level, mg/L (Serum nl , 0.9) *Articular Surface Replacement implants (ASR): metal-on-metal Co-Cr hip implant by DePuy Orthopaedics; internationally recalled in 2010. CSF, cerebrospinal fluid; EMG, electromyogram; EOG, electrooculogram; ERG, electroretinography; mfERG, multifocal electroretinography; mfVEP, multifocal visual evoked potentials; MRI, magnetic resonance imaging; OCT, optical coherence tomography; OD, right eye; OS, left eye; OU, both eyes; RPE, retinal pigment epithelium; VA, visual acuity; VEP, visual evoked potential; VF, visual field. 385 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. TABLE 1. Cases of ocular cobalt toxicity localized to the optic nerve 386 Weber et al (5) *Articular Surface Replacement implants (ASR): metal-on-metal Co-Cr hip implant by DePuy Orthopaedics; internationally recalled in 2010. ERG, electroretinography; OCT, optical coherence tomography; OD, right eye; OS, left eye; OU, both eyes; RPE, retinal pigment epithelium; VEP, visual evoked potential; VF, visual field. 14 Blood: 411 Decline in vision, general malaise, pericardiomyopathy, hypothyroidism, motor axonopathy Visual and hearing loss, depression, weight loss, paresthesias in hands and feet, imbalance Plasma: 446.4 Apel et al (4,6) Bilateral metal-onmetal hip arthroplasty (ASR system, DePuy*) Metal-on-ceramic hip arthroplasty (DePuy femoral head) Metal-on-ceramic hip arthroplasty Ng et al (3) 48 Paracentral scotoma in OS, dysgeusia Type of Exposure Case Report Serum: 44.6 Symptoms, Examination Findings, and Ancillary Tests Highest Measured Cobalt Level in mg/L (Serum Normal ,0.9) Time to Symptom Onset in months TABLE 2. Cases of ocular cobalt toxicity localized to the retina The origin of visual loss due to cobalt toxicity has long been debated. Currently, 5 case studies reported optic nerve atrophy based on fundus examination, of which 2 reported abnormal VEP testing (Table 1). An additional case was reported with an abnormal VEP, but did not include a fundus examination (1,2). None of these cases had ERG testing. In contrast, 3 cases found retinal toxicity, 2 with abnormal ERG and 1 with photoreceptor thinning on OCT (Table 2). Two of these 3 reported normal VEP testing, isolating toxicity to the retina (3,4). Our case stands in contrast to the recently reported cases of retinal cobalt toxicity. Weber et al (5) described a woman with a history of hip prosthesis and decreased vision in both eyes with an ISCEV standard full-field ERG showing significant cone dysfunction. Similarly, Apel et al (4,6) reported a case of arthroprosthetic cobaltism with persistent abnormalities in all phases of ERG including a negative bwaveform, suggesting inner retinal pathology. In contrast, the ISCEV standard full-field ERG conducted on our patient's nonamblyopic eye showed normal flicker timing and amplitude, with both photopic and scotopic waveforms within normal limits (see Supplemental Digital Content, Figure E2, http://links.lww.com/WNO/A200). In addition, the multifocal ERG showed amplitudes and latencies within normal limits (see Supplemental Digital Content, Figure E3, http://links.lww.com/WNO/A201), and the OCT of the macula reveals the outer retinal layers to be of normal shape and contour (see Supplemental Digital Content, Figure E1, http://links.lww.com/WNO/A199). Therefore, we conclude that it is unlikely that the outer layers of the retina have been affected by cobalt toxicity. The decreased central amplitudes of the mfVEP are consistent with dysfunction somewhere along the anterior or posterior visual pathways. Because the mfVEP tests macular function, we cannot fully rule out early retinal toxicity that has yet to manifest on the mfERG or full-field ERG. However, the cecocentral depression on VF testing and loss of color vision out of proportion to reduced visual acuity are most consistent with a toxic optic neuropathy (14). Although the OCT demonstrated that inner retinal layers (RNFL and RGC-IPL) were of normal thickness, it is Tissue Abnormality DISCUSSION 24 Visual Tests cobalt-chromium prosthesis showed significant wear of the head, and metal infiltrates were found on the acetabular cup. The cobalt level measured in the synovial fluid exceeded the maximum recordable value of 1,000.0 mg/L. Ten weeks later, the cobalt level in the patient's serum had decreased to 55.9 mg/L. Twelve weeks after surgery, visual acuity was 20/30, left eye, and the patient could recognize 3 of 6 color plates. By 18 months after surgery, left visual acuity was 20/25, his vision continued to improve, and the left VF was normal. His serum cobalt level was 7.4 mg/L. Chorioretinal Normal VEP, normal ERG (slightly degeneration; RPE reduced amplitudes OS compared dysfunction OS with OD) OCT: degenerative alterations of RPE in OS Retinopathy Abnormal photopic and scotopic ERG, normal VEP; 18 mo after revision: ERG improved to near normal, VEP: delays OU Retinopathy VF: bilateral central scotoma; ERG: severe cone dysfunction Original Contribution Grillo et al: J Neuro-Ophthalmol 2016; 36: 383-388 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution possible that toxic damage to the ganglion cells and their axons had not yet resulted in thinning. Possibly our patient had thick RNFL and RGC+ layers that did not show demonstrable loss of fibers at the time of OCT testing. We conclude that we may have detected an early stage of optic nerve toxicity that is not yet structurally apparent on OCT. Proposed mechanisms of cobalt toxicity may explain involvement of both the optic nerve and retina. Optic neuropathy due to cobalt toxicity is attributed to defective mitochondrial oxidative phosphorylation, similar to that seen in Leber hereditary optic neuropathy and dominant optic atrophy (15). Because RGCs lack myelin, they may be prone to damage from mitochondrial dysfunction, where defects in the respiratory chain lead to oxidative stress and, ultimately, apoptosis (16). Cobalt also is known to block calcium-dependent synaptic transmission between photoreceptors and second-order neurons, inhibiting the negative feedback in the outer retina that leads to glutamate release to bipolar and horizontal cells (17). Animal studies have shown evidence of cobalt toxicity in both the retina and the optic nerve. Cobalt was found to suppress rod signal transmission in the outer plexiform layer in super-perfused, isolated carp retina and diminish the rod- and cone-driven b-wave responses in frog retina (18). Evans et al (19) showed complete elimination of rod photoreceptor contribution to the ERG bwave in frog retina exposed to cobalt. Hara et al (20) found photoreceptor cells progressively underwent apoptosis with time and under dose-response relationship after intravitreal injections of cobalt chloride in mice and rats. In contrast, Apostoli et al (16) found severe ganglion cell depletion, diffuse areas of optic nerve damage, and axonal swelling after daily dosage of rabbits with intravenous cobalt, with severity of damage related to dose and time of exposure. Only a portion of patients with high serum cobalt levels develop symptoms of toxicity, and these symptoms vary from patient to patient. This may be due to albumin binding capacity, which affects the amount of free cobalt in the blood and generation of free radicals by cobalt (21). In addition, as cobalt toxicity has been linked to mitochondrial dysfunction, it is possible that some patients may develop a compensating increase in mitochondrial mass and are less susceptible to cobalt toxicity, just as unaffected carriers of the Leber genotype were found to have a greater mitochondrial mass when compared with their affected relatives (22). In conclusion, a normal ERG in a patient with history of metal-on-metal hip prosthesis does not rule out cobalt toxicity, particularly when it is accompanied by other symptoms, such as tinnitus, deafness, peripheral neuropathy, incoordination, depression, cardiomyopathy, and hypothyroidism (2). It is important to perform a complete workup, including ISCEV standard full-field ERG, Grillo et al: J Neuro-Ophthalmol 2016; 36: 383-388 mfERG, mfVEP, and OCT in patients losing sight and suspected of having cobalt toxicity. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: L. Grillo, D. C. Hood, H. V. Nguyen, J. G. Odel, S. H. Tsang; b. Acquisition of data: L. Grillo, H. V. Nguyen, J. G. Odel, S. H. Tsang; c. Analysis and interpretation of data: L. Grillo, D. C. Hood, H. V. Nguyen, J. G. Odel, S. H. Tsang. Category 2: a. Drafting the manuscript: L. Grillo, D. C. Hood, H. V. Nguyen, J. G. Odel, S. H. Tsang; b. Revising it for intellectual content: L. Grillo, D. C. Hood, H. V. Nguyen, Jeffrey Odel, S. H. Tsang. Category 3: a. Final approval of the completed manuscript: L. Grillo, D. C. Hood, H. V. Nguyen, Jeffrey Odel, S. H. Tsang. REFERENCES 1. Rizzetti M, Liberini P, Zarattini G, Catalani S, Pazzaglia U, Apostoli P, Padovani A. Loss of sight and sound. 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Efficient mitochondrial biogenesis drives incomplete penetrance in Leber's hereditary optic neuropathy. Brain. 2014;137:335-353. Buried in the "et al" David H. Johnson, MD, MACP, FASCO Buried in the "et al". .better than the "not at all"? I made a contribution, but got no attribution. I listened to the presentation, .and there was no hesitation, to take the credit and the fame; I never even heard my name. Life is not always fair, a truth I must humbly bear, as pride goes before a fall, .buried in the "et al". Reprinted with permission from the Alpha Omega Alpha quarterly journal The Pharos. Dr. Johnson lives in Dallas, Texas. 388 Grillo et al: J Neuro-Ophthalmol 2016; 36: 383-388 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.