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Review

Neuro-Ophthalmic Manifestations of HIV Infection

, MD, PhD & , MBChB, FRANZCO, MD, PhD
Pages 1085-1093 | Received 09 Aug 2019, Accepted 09 Dec 2019, Published online: 21 Jan 2020

References

  • Jabs DA, Green WR, Fox R, Polk BF, Bartlett JG. Ocular manifestations of acquired immune deficiency syndrome. Ophthalmology. 1989;96(7):1092–1099. doi:10.1016/S0161-6420(89)32794-1.
  • Feroze KB, Wang J. Ocular manifestations of HIV. In: StatPearls. Treasure Island (FL): StatPearls Publishing StatPearls Publishing LLC; 2019.
  • Ng WT, Versace P. Ocular association of HIV infection in the era of highly active antiretroviral therapy and the global perspective. Clin Exp Ophthalmol. 2005;33(3):317–329. doi:10.1111/ceo.2005.33.issue-3.
  • Murray CJ, Ortblad KF, Guinovart C, et al. Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990-2013: a systematic analysis for the global burden of disease study 2013. Lancet. 2014;384(9947):1005–1070. doi:10.1016/S0140-6736(14)60844-8.
  • Freeman WR, Van Natta ML, Jabs D, et al. Vision function in HIV-infected individuals without retinitis: report of the studies of ocular complications of AIDS research group. Am J Ophthalmol. 2008;145(3):453–462. doi:10.1016/j.ajo.2007.10.013.
  • Friedman DI. Neuro-ophthalmic manifestations of human immunodeficiency virus infection. Neurol Clin. 1991;9(1):55–72. doi:10.1016/S0733-8619(18)30303-7.
  • Keane JR. Neuro-ophthalmologic signs of AIDS: 50 patients. Neurology. 1991;41(6):841–845. doi:10.1212/WNL.41.6.841.
  • Mwanza JC, Nyamabo LK, Tylleskar T, Plant GT. Neuro-ophthalmological disorders in HIV infected subjects with neurological manifestations. Br J Ophthalmol. 2004;88(11):1455–1459. doi:10.1136/bjo.2004.044289.
  • Jabs DQT. Acquired immunodeficiency syndrome. In: Pepose JHG, Wilhelmus K, eds. Ocular Infection and Immunity. St Louis: Mosby- Year Book; 1996:289–310.
  • Gray F, Adle-Biassette H, Chretien F, Lorin de la Grandmaison G, Force G, Keohane C. Neuropathology and neurodegeneration in human immunodeficiency virus infection. Pathogenesis of HIV-induced lesions of the brain, correlations with HIV-associated disorders and modifications according to treatments. Clin Neuropathol. 2001;20:146–155.
  • Sheikh HU, Cho TA. Clinical aspects of headache in HIV. Headache. 2014;54(5):939–945. doi:10.1111/head.2014.54.issue-5.
  • Joshi SG, Cho TA. Pathophysiological mechanisms of headache in patients with HIV. Headache. 2014;54(5):946–950. doi:10.1111/head.2014.54.issue-5.
  • Kirkland KE, Kirkland K, Many WJ Jr., Smitherman TA. Headache among patients with HIV disease: prevalence, characteristics, and associations. Headache. 2012;52(3):455–466. doi:10.1111/j.1526-4610.2011.02025.x.
  • Krasenbaum LJ. A review of HIV and headache: A cross-sectional study. Headache. 2017;57(10):1631–1632. doi:10.1111/head.13222.
  • Creamer A, Ioannidis S, Wilhelm T, Mahungu T, Lipman M. Headache in an HIV positive patient: diagnostic challenges and approach to treatment. Clin Med (Lond). 2016;16(6):548–550. doi:10.7861/clinmedicine.16-6-548.
  • Wells CD, Moodley AA. HIV-associated cavernous sinus disease. South Afr J HIV Med. 2019;20(1):862. doi:10.4102/sajhivmed.v20i1.862.
  • Sohail S, Nakigozi G, Anok A, et al. Headache prevalence and its functional impact among HIV-infected adults in rural Rakai District, Uganda. J Neurovirol. 2019;25(2):248–253. doi:10.1007/s13365-018-0710-9.
  • Sampaio Rocha-Filho PA, Torres RCS, Ramos Montarroyos U. HIV and headache: A cross-sectional study. Headache. 2017;57(10):1545–1550. doi:10.1111/head.13183.
  • Evers S, Wibbeke B, Reichelt D, Suhr B, Brilla R, Husstedt I. The impact of HIV infection on primary headache. Unexpected findings from retrospective, cross-sectional, and prospective analyses. Pain. 2000;85(1–2):191–200. doi:10.1016/S0304-3959(99)00266-3.
  • Stewart MW. Human immunodeficiency virus and its effects on the visual system. Infect Dis Rep. 2012;4(1):e25. doi:10.4081/idr.2012.3853.
  • Sadun AA, Pepose JS, Madigan MC, Laycock KA, Tenhula WN, Freeman WR. AIDS-related optic neuropathy: a histological, virological and ultrastructural study. Graefes Arch Clin Exp Ophthalmol. 1995;233(7):387–398. doi:10.1007/BF00180941.
  • Goldsmith P, Jones RE, Ozuzu GE, Richardson J, Ong EL. Optic neuropathy as the presenting feature of HIV infection: recovery of vision with highly active antiretroviral therapy. Br J Ophthalmol. 2000;84(5):551–553. doi:10.1136/bjo.84.5.546g.
  • Apinyawasisuk S, Poonyathalang A, Preechawat P, Vanikieti K. Syphilitic optic neuropathy: re-emerging cases over a 2-year period. Neuroophthalmology. 2016;40(2):69–73. doi:10.3109/01658107.2015.1134586.
  • Cackett P, Weir CR, McFadzean R, Seaton RA. Optic neuropathy without retinopathy in AIDS and cytomegalovirus infection. J Neuroophthalmol. 2004;24(1):94–95. doi:10.1097/00041327-200403000-00030.
  • Golnik KC, Newman SA, Wispelway B. Cryptococcal optic neuropathy in the acquired immune deficiency syndrome. J Clin Neuroophthalmol. 1991;11:96–103.
  • Hughes EH, Petrushkin H, Sibtain NA, Stanford MR, Plant GT, Graham EM. Tuberculous orbital apex syndromes. Br J Ophthalmol. 2008;92(11):1511–1517. doi:10.1136/bjo.2008.138974.
  • Klein A, Fischer N, Goldstein M, Shulman S, Habot-Wilner Z. The great imitator on the rise: ocular and optic nerve manifestations in patients with newly diagnosed syphilis. Acta Ophthalmol. 2019;97(4): e641-e647. doi:10.1111/aos.13963.
  • Wadood AC, Dhillon B, McIlwaine G, Brettle RP. Delayed diagnosis of HIV infection in ophthalmic practice. Eye (Lond). 2004;18(3):293–298. doi:10.1038/sj.eye.6700630.
  • Babu K, Murthy KR, Rajagopalan N, Satish B. Vision recovery in human immunodeficiency virus-infected patients with optic neuropathy treated with highly active antiretroviral therapy: a case series. Indian J Ophthalmol. 2009;57(4):315–318. doi:10.4103/0301-4738.53062.
  • Bell JE. An update on the neuropathology of HIV in the HAART era. Histopathology. 2004;45(6):549–559. doi:10.1111/his.2004.45.issue-6.
  • Almekhlafi MA, Williams G, Costello F. Clinical reasoning: optic disc swelling in a patient with AIDS. Neurology. 2011;77(5):e28–32. doi:10.1212/WNL.0b013e318227b1d4.
  • Bergemann A, Karstaedt AS. The spectrum of meningitis in a population with high prevalence of HIV disease. Qjm. 1996;89(7):499–504. doi:10.1093/qjmed/89.7.499.
  • Espino Barros Palau A, Morgan ML, Foroozan R, Lee AG. Neuro-ophthalmic presentations and treatment of cryptococcal meningitis-related increased intracranial pressure. Can J Ophthalmol. 2014;49(5):473–477. doi:10.1016/j.jcjo.2014.06.012.
  • Merkler AE, Gaines N, Baradaran H, et al. Direct invasion of the optic nerves, chiasm, and tracts by cryptococcus neoformans in an immunocompetent host. Neurohospitalist. 2015;5(4):217–222. doi:10.1177/1941874415569072.
  • Merkler AE, Reynolds AS, Gialdini G, et al. Neurological complications after tuberculous meningitis in a multi-state cohort in the United States. J Neurol Sci. 2017;375:460–463. doi:10.1016/j.jns.2017.02.051.
  • Moodley A, Rae W, Bhigjee A. Visual loss in HIV-associated cryptococcal meningitis: A case series and review of the mechanisms involved. South Afr J HIV Med. 2015;16(1):305. doi:10.4102/sajhivmed.v16i1.305.
  • Veltman JA, Bristow CC, Klausner JD. Meningitis in HIV-positive patients in sub-Saharan Africa: a review. J Int AIDS Soc. 2014;17:19184. doi:10.7448/IAS.17.1.19184.
  • Rajasingham R, Rhein J, Klammer K, et al. Epidemiology of meningitis in an HIV-infected Ugandan cohort. Am J Trop Med Hyg. 2015;92(2):274–279. doi:10.4269/ajtmh.14-0452.
  • Moodley A, Rae W, Bhigjee A, et al. Early clinical and subclinical visual evoked potential and humphrey’s visual field defects in cryptococcal meningitis. PLoS One. 2012;7(12):e52895. doi:10.1371/journal.pone.0052895.
  • Torok ME. Tuberculous meningitis: advances in diagnosis and treatment. Br Med Bull. 2015;113(1):117–131. doi:10.1093/bmb/ldv003.
  • Marais BJ, Heemskerk AD, Marais SS, et al. Standardized methods for enhanced quality and comparability of tuberculous meningitis studies. Clin Infect Dis. 2017;64(4):501–509. doi:10.1093/cid/ciw757.
  • Benjamin LA, Kelly M, Cohen D, et al. Detection of herpes viruses in the cerebrospinal fluid of adults with suspected viral meningitis in Malawi. Infection. 2013;41(1):27–31. doi:10.1007/s15010-012-0292-z.
  • Franco-Paredes C, Bellehemeur T, Merchant A, Sanghi P, DiazGranados C, Rimland D. Aseptic meningitis and optic neuritis preceding varicella-zoster progressive outer retinal necrosis in a patient with AIDS. Aids. 2002;16(7):1045–1049. doi:10.1097/00002030-200205030-00011.
  • Goldberg DE, Smithen LM, Angelilli A, Freeman WR. HIV-associated retinopathy in the HAART era. Retina. 2005;25(5):633–649. quiz 682-633. doi:10.1097/00006982-200507000-00015.
  • Furrer H, Barloggio A, Egger M, Garweg JG. Retinal microangiopathy in human immunodeficiency virus infection is related to higher human immunodeficiency virus-1 load in plasma. Ophthalmology. 2003;110(2):432–436. doi:10.1016/S0161-6420(02)01750-5.
  • Pivetti-Pezzi P, Accorinti M, Ciapparoni V, Vullo V, Aiuti F. Antiretroviral therapy and HIV-related retinal microangiopathy. Aids. 1997;11(15):1890–1891. doi:10.1097/00002030-199715000-00019.
  • Iwasaki Y, Yamamoto N, Kawaguchi T, et al. Human immunodeficiency virus-related retinal microangiopathy and systemic cytomegalovirus disease association. Jpn J Ophthalmol. 2013;57(4):372–378. doi:10.1007/s10384-013-0247-7.
  • Nishijima T, Yashiro S, Teruya K, et al. Routine eye screening by an ophthalmologist is clinically useful for HIV-1-infected patients with CD4 count less than 200/μL. PLoS One. 2015;10(9):e0136747. doi:10.1371/journal.pone.0136747.
  • Dadgostar H, Holland GN, Huang X, et al. Hemorheologic abnormalities associated with HIV infection: in vivo assessment of retinal microvascular blood flow. Invest Ophthalmol Vis Sci. 2006;47(9):3933–3938. doi:10.1167/iovs.06-0138.
  • Jabs DA, Drye L, Van Natta ML, Thorne JE, Holland GN. Incidence and long-term outcomes of the human immunodeficiency virus neuroretinal disorder in patients with AIDS. Ophthalmology. 2015;122(4):760–768. doi:10.1016/j.ophtha.2014.11.009.
  • Wang HH, Chung YM, Lin YC, Hu HC, Wong WW. Rifabutin-induced hypopyon uveitis in patients with acquired immunodeficiency syndrome infected with mycobacterium avium complex. J Chin Med Assoc. 2007;70(3):136–139. doi:10.1016/S1726-4901(09)70345-4.
  • Riva A, Invernizzi A, Resnati C, Micheli V, Cattaneo D, Gervasoni C. Elvitegravir/cobicistat-associated toxic optical neuropathy in an HIV-infected patient: a call for caution? Antivir Ther. 2017;22(5):453–455. doi:10.3851/IMP3058.
  • Demirkaya N, Wit F, Schlingemann R, Verbraak F. Neuroretinal degeneration in HIV patients without opportunistic ocular infections in the cART Era. AIDS Patient Care STDS. 2015;29(10):519–532. doi:10.1089/apc.2015.0091.
  • Gellrich MM, Kade G, Gerling J, Bach M, Hansen LL. Pattern, flicker, and flash electroretinography in human immunodeficiency virus infection: a longitudinal study. Ger J Ophthalmol. 1996;5(1):16–22.
  • Currie J, Benson E, Ramsden B, Perdices M, Cooper D. Eye movement abnormalities as a predictor of the acquired immunodeficiency syndrome dementia complex. Arch Neurol. 1988;45(9):949–953. doi:10.1001/archneur.1988.00520330027006.
  • Johnston JL, Miller JD, Nath A. Ocular motor dysfunction in HIV-1-infected subjects: a quantitative oculographic analysis. Neurology. 1996;46(2):451–457. doi:10.1212/WNL.46.2.451.
  • Maclean H, Dhillon B. Pupil cycle time and human immunodeficiency virus (HIV) infection. Eye (Lond). 1993;7(Pt 6):785–786. doi:10.1038/eye.1993.184.
  • Urban B, Bakunowicz-Lazarczyk A, Michalczuk M. Immune recovery uveitis: pathogenesis, clinical symptoms, and treatment. Mediators Inflamm. 2014;2014:971417. doi:10.1155/2014/971417.
  • Nguyen QD, Kempen JH, Bolton SG, Dunn JP, Jabs DA. Immune recovery uveitis in patients with AIDS and cytomegalovirus retinitis after highly active antiretroviral therapy. Am J Ophthalmol. 2000;129(5):634–639. doi:10.1016/S0002-9394(00)00356-1.
  • Prevention CfDCa. https://www.cdc.gov/tb/publications/guidelines/hiv_aids.htm. Published 2018. Accessed November, 2019.
  • Chamberlain PD, Sadaka A, Berry S, Lee AG. Ethambutol optic neuropathy. Curr Opin Ophthalmol. 2017;28(6):545–551. doi:10.1097/ICU.0000000000000416.
  • Cheng WH, Chang CH, Lu PL, Lin HC. Bilateral uveitis associated with concurrent administration of rifabutin and nelfinavir. Taiwan J Ophthalmol. 2015;5(4):187–188. doi:10.1016/S0161-6420(85)34008-3.
  • Bowen LN, Smith B, Reich D, Quezado M, Nath A. HIV-associated opportunistic CNS infections: pathophysiology, diagnosis and treatment. Nat Rev Neurol. 2016;12(11):662–674. doi:10.1038/nrneurol.2016.149.
  • Peeling RW, Hook EW 3rd. The pathogenesis of syphilis: the great mimicker, revisited. J Pathol. 2006;208(2):224–232. doi:10.1002/(ISSN)1096-9896.
  • Berger JR, Dean D. Neurosyphilis. Handb Clin Neurol. 2014;121:1461–1472.
  • Hook EW 3rd. Syphilis. Lancet. 2017;389(10078):1550–1557. doi:10.1016/S0140-6736(16)32411-4.
  • Merins V, Hahn K. Syphilis and neurosyphilis: HIV-coinfection and value of diagnostic parameters in cerebrospinal fluid. Eur J Med Res. 2015;20:81. doi:10.1186/s40001-015-0175-8.
  • Davis AP, Stern J, Tantalo L, et al. How well do neurologic symptoms identify individuals with neurosyphilis? Clin Infect Dis. 2018;66(3):363–367. doi:10.1093/cid/cix799.
  • Bhatti MT. Optic neuropathy from viruses and spirochetes. Int Ophthalmol Clin. 2007;47(4):37–66, ix. doi:10.1097/IIO.0b013e318157202d.
  • Fonollosa A, Martinez-Indart L, Artaraz J, et al. Clinical manifestations and outcomes of syphilis-associated Uveitis in Northern Spain. Ocul Immunol Inflamm. 2016;24(2):147–152. doi:10.3109/09273948.2014.943349.
  • Chesson HW, Heffelfinger JD, Voigt RF, Collins D. Estimates of primary and secondary syphilis rates in persons with HIV in the United States, 2002. Sex Transm Dis. 2005;32(5):265–269. doi:10.1097/01.olq.0000162359.75509.9c.
  • Hobbs E, Vera JH, Marks M, Barritt AW, Ridha BH, Lawrence D. Neurosyphilis in patients with HIV. Pract Neurol. 2018;18(3):211–218. doi:10.1136/practneurol-2017-001754.
  • Golden MR, Marra CM, Holmes KK. Update on syphilis: resurgence of an old problem. Jama. 2003;290(11):1510–1514. doi:10.1001/jama.290.11.1510.
  • Marra CM, Gary DW, Kuypers J, Jacobson MA. Diagnosis of neurosyphilis in patients infected with human immunodeficiency virus type 1. J Infect Dis. 1996;174(1):219–221. doi:10.1093/infdis/174.1.219.
  • Taylor MM, Aynalem G, Olea LM, He P, Smith LV, Kerndt PR. A consequence of the syphilis epidemic among men who have sex with men (MSM): neurosyphilis in Los Angeles, 2001-2004. Sex Transm Dis. 2008;35(5):430–434. doi:10.1097/OLQ.0b013e3181644b5e.
  • Stevenson J, Heath M. Syphilis and HIV infection: an update. Dermatol Clin. 2006;24(4):497–507, vi. doi:10.1016/j.det.2006.06.013.
  • Tucker JD, Li JZ, Robbins GK, et al. Ocular syphilis among HIV-infected patients: a systematic analysis of the literature. Sex Transm Infect. 2011;87(1):4–8. doi:10.1136/sti.2010.043042.
  • Northey LC, Skalicky SE, Gurbaxani A, McCluskey PJ. Syphilitic uveitis and optic neuritis in Sydney, Australia. Br J Ophthalmol. 2015;99(9):1215–1219. doi:10.1136/bjophthalmol-2014-306168.
  • Fonollosa A, Giralt J, Pelegrin L, et al. Ocular syphilis–back again: understanding recent increases in the incidence of ocular syphilitic disease. Ocul Immunol Inflamm. 2009;17(3):207–212. doi:10.1080/09273940902741709.
  • Marra CM, Tantalo LC, Maxwell CL, Dougherty K, Wood B. Alternative cerebrospinal fluid tests to diagnose neurosyphilis in HIV-infected individuals. Neurology. 2004;63(1):85–88. doi:10.1212/01.WNL.0000131902.69113.34.
  • Pepose JS, Holland GN, Nestor MS, Cochran AJ, Foos RY. Acquired immune deficiency syndrome. Pathogenic mechanisms of ocular disease. Ophthalmology. 1985;92:472–484.
  • Skipper C, Abassi M, Boulware DR. Diagnosis and management of central nervous system cryptococcal infections in HIV-infected adults. J Fungi (Basel). 2019;5(3):65.
  • WHO guidelines approved by the guidelines review committee. In: Guidelines for the Diagnosis, Prevention and Management of Cryptococcal Disease in HIV-Infected Adults, Adolescents and Children: Supplement to the 2016 Consolidated Guidelines on the Use of Antiretroviral Drugs for Treating and Preventing HIV Infection. Geneva: World Health Organization (c) World Health Organization; 2018.
  • Beare NA, Kublin JG, Lewis DK, et al. Ocular disease in patients with tuberculosis and HIV presenting with fever in Africa. Br J Ophthalmol. 2002;86(10):1076–1079. doi:10.1136/bjo.86.10.1076.
  • Sudharshan S, Kaleemunnisha S, Banu AA, et al. Ocular lesions in 1,000 consecutive HIV-positive patients in India: a long-term study. J Ophthalmic Inflamm Infect. 2013;3(1):2. doi:10.1186/1869-5760-3-2.
  • Moorthy RS, Smith RE, Rao NA. Progressive ocular toxoplasmosis in patients with acquired immunodeficiency syndrome. Am J Ophthalmol. 1993;115(6):742–747. doi:10.1016/S0002-9394(14)73641-4.
  • Falcone PM, Notis C, Merhige K. Toxoplasmic papillitis as the initial manifestation of acquired immunodeficiency syndrome. Ann Ophthalmol. 1993;25:56–57.
  • Wei ME, Campbell SH, Taylor C. Precipitous visual loss secondary to optic nerve toxoplasmosis as an unusual presentation of AIDS. Aust N Z J Ophthalmol. 1996;24(1):75–77. doi:10.1111/ceo.1996.24.issue-1.
  • Lee MW, Fong KS, Hsu LY, Lim WK. Optic nerve toxoplasmosis and orbital inflammation as initial presentation of AIDS. Graefes Arch Clin Exp Ophthalmol. 2006;244(11):1542–1544. doi:10.1007/s00417-006-0295-5.
  • Adang L, Berger J. Progressive multifocal leukoencephalopathy. F1000Res. 2015;4. doi:10.12688/f1000research.7071.1.
  • Richardson EP Jr. Progressive multifocal leukoencephalopathy 30 years later. N Engl J Med. 1988;318(5):315–317. doi:10.1056/NEJM198802043180510.
  • Ormerod LD, Rhodes RH, Gross SA, Crane LR, Houchin KW. Ophthalmologic manifestations of acquired immune deficiency syndrome-associated progressive multifocal leukoencephalopathy. Ophthalmology. 1996;103(6):899–906. doi:10.1016/S0161-6420(96)30589-7.
  • Gopal S, Martin KE, Richards KL, Eron JJ. Clinical presentation, treatment, and outcomes among 65 patients with HIV-associated lymphoma treated at the University of North Carolina, 2000-2010. AIDS Res Hum Retroviruses. 2012;28(8):798–805. doi:10.1089/aid.2011.0259.
  • Ji Y, Lu H. Malignancies in HIV-infected and AIDS patients. Adv Exp Med Biol. 2017;1018:167–179.
  • Lilly AJ, Fedoriw Y. Human immunodeficiency virus-associated lymphoproliferative disorders. Surg Pathol Clin. 2019;12(3):771–782. doi:10.1016/j.path.2019.03.005.
  • Brandsma D, Bromberg JEC. Primary CNS lymphoma in HIV infection. Handb Clin Neurol. 2018;152:177–186.
  • Hwang CS, Yeh S, Bergstrom CS. Diagnostic vitrectomy for primary intraocular lymphoma: when, why, how? Int Ophthalmol Clin. 2014;54(2):155–171. doi:10.1097/IIO.0000000000000022.
  • Castillo JJ, Bibas M, Miranda RN. The biology and treatment of plasmablastic lymphoma. Blood. 2015;125(15):2323–2330. doi:10.1182/blood-2014-10-567479.
  • Morley AM, Verity DH, Meligonis G, Rose GE. Orbital plasmablastic lymphoma–comparison of a newly reported entity with diffuse large B-cell lymphoma of the orbit. Orbit. 2009;28(6):425–429. doi:10.3109/01676830903177427.

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