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Show Journal of Nemo- Ophthalmology 14( 1): 15- 20, 1994. © 1994 Raven Press, Ltd., New York Ophthalmic Manifestations in Lyme Borreliosis A Review J. Bergloff, M. D., R. Gasser, M. D., Ph. D., and B. Feigl, M. D. Lyme borreliosis is an emerging tickborne spirochetal infection characterized by a broad variety of symptoms, ranging from neurologic disorders and different skin manifestations to cardiac symptoms. Many ocular and neuro- ophthalmic symptoms have recently been attributed to Lyme disease. Especially in endemic areas ophthalmologists need to be aware of Borrelia burgdorferi as a possible causal agent. The aim of this paper is to present a short review of the literature of ophthalmic disorders resulting from Borrelia burgdorferi infections. Key Words: Borrelia burgdorferi- Lyme disease- eye- ophthalmic. From the Departments of Ophthalmology ( J. B., B. F.) and Internal Medicine ( R. G.), University of Graz, Austria. Address correspondence and reprint requests to Dr. Jutta Bergloff, Department of Ophthalmology, University of Graz, Auenbruggerplace 4, 8036 Graz, Austria. During recent years, there has been a growing awareness of Lyme borreliosis. Borrelia burgdorferi infection can be associated with a variety of symptoms, including neurologic, dermatologic, cardiac, and ophthalmic disorders. The infectious agent causing Lyme disease is the spirochete Borrelia burgdorferi, which is transmitted by Ixodes ticks ( 1 - 3). Recently, B. burgdorferi has also been found in mosquitoes and deer flies ( 4). Lyme borreliosis is found throughout the Americas, Europe, and Asia ( 4). The clinical course of Lyme disease has been divided into three stages ( 1,5- 7). Stage I directly follows the bite by an infected tick. Patients develop a typical skin lesion, erythema chronicum migrans ( 8) and, sometimes, nonspecific influenzalike symptoms and fever. After several weeks, spirochetes spread in the body and patients may develop neurologic symptoms and skin and cardiac manifestations ( stage II) ( 5,9- 12). Stage III is mainly characterized by polyarthritis, progressive encephalomyelitis- similar to multiple sclerosis ( 1, 5,9,11), and skin disorders with acrodermatitis chronica atrophicans ( 13). But not every patient follows this course ( 8,14,15). There is, in fact, no clear line to be drawn between the three stages, neither with respect to time of occurrence nor to symptoms. B. burgdorferi has been isolated from blood, from cerebrospinal fluid, and from various tissues ( 10, 16). Although Borrelia has also been identified histologically in the retina and in the vitreous humor ( 17- 19), little attention has been focused on the ophthalmic manifestations of Lyme borreliosis. At the Fifth International Conference on Lyme Borreliosis, only 1 of 400 oral presentations was devoted to intraocular manifestations of Lyme disease ( 20). Since Lyme disease can be associated with a number of ophthalmic manifestations, B. burgdorferi should be considered as a possible causal agent. 15 16 ]. BERGLOFF FT AF. The aim of this article is to review the reported ophthalmic disorders associated with B. burgdorferi infection. OPHTHALMIC MANIFESTATIONS OF BORRELIA BURGDORFERI INFECTION Ophthalmic Manifestations in Stage I See Table 1. Conjunctivitis, Periorbital Edema, and Photophobia Follicular conjunctivitis with photophobia and periorbital edema have been observed in 11% of patients in the early stages of Lyme disease ( 1,16,17,21- 23). Ophthalmic Manifestations in Stage II See Table 2. Uveitis Iridocyclitis. Several case reports of Lyme disease and granulomatous iritis with posterior synechia have been published ( 1,7,9,17- 19,24- 34). Kauffmann and Wormser ( 18) have shown that panuveitis with disseminated chorioretinitis may follow iridocyclitis. Pars Planitis. Chronic intermediate uveitis with classic snowbanking and severe cystoid macular edema has been reported by Breeveld and associates ( 21). In spite of the fact that the patient had suffered for 10 years, the ocular symptoms responded promptly to intravenous antibiotic therapy. Another case of pars planitis associated with facial paralysis has been presented by Winward and colleagues ( 7). Other studies of pars planitis have appeared recently ( 25,26,28,30,35,36). Vitritis. Kuiper and colleagues ( 37) observed vitritis in association with Lyme meningitis and cranial polyneuritis 6 weeks after a tick bite causing erythema migrans. Although a single case report, it demonstrates the variety of ophthalmic manifestations of Lyme borreliosis. Winward and colleagues ( 7) described several patients with positive laboratory findings of borreliosis who had recurrent bilateral vitritis and granulomatous iridocyclitis, relatively resistant to therapy. Other studies of vitritis have been published ( 21,28,30). Chorioiditis. Two cases of bilateral diffuse chorioiditis, cystoid macular edema and exudative retinal detachment have been described ( 1,26,38, 39). These patients also suffered from lymphocytic meningitis secondary to Lyme disease. The dramatic improvement of ocular complaints in these patients after doxycycline therapy suggests borreliosis as a possible cause. Pigmentepitheliitis: Bialasiewicz and coworkers ( 40) observed a patient with hyper- and depigmentations in the macular region in association with Borrelia burgdorferi seroconversion. It was similar to pigmentepitheliitis. Further investigations will have to prove the relevance of this coincidence. Acute Multifocal Posterior Placoid Pigmentepi-thiopathy ( AMPPPE). AMPPPE is an idiopathic chorioretinal inflammation. Viral infections etiology has been postulated ( 41). Recently, Wiegand ( 31), and Tonjes and colleagues ( 42) described cases of presumed AMPPPE in association with Lyme disease. Retinal Vasculitis. Several cases of retinal vasculitis in Lyme disease associated with vitritis and pars planitis have been presented ( 1,26,30,33,43). One patient with positive serology for Borrelia burgdorferi developed retinal neovascularization and cystoid macular edema. He received oral tetracycline therapy and improved markedly. In two other cases of severe retinal vasculitis associated with B. burgdorferi infection, medical and surgical therapy was applied after antibiotic treatment was not successful ( 30). It is not unexpected that retinal vasculitis may occur in Lyme disease, since similar findings are frequently seen in the later stages of syphilis, another spirochetal infection ( 30). Endophthalmitis Kauffmann and colleagues ( 18,19) described a patient who showed severe unilateral panendoph- TABLE 1. Stage I ( 4- 8 weeks) Ocular symptoms Systemic symptoms Routine serology Conjunctivitis Periorbital edema Photophobia Primary effect Erythema chronicum migrans Lymphadenosis cutis benigna Generalization Fever, malaise, headache IgG: negative IgM: negative Data from Refs. 5, 9, and 10. J Neuro- Ophtlmlmol, Vol. 14, No. 1, 1994 MANIFESTATIONS IN LYME BORRELIOSIS 17 TABLE 2. Stage II (< 1 year) Ocular symptoms Systemic symptoms Routine serology Uveitis Iridocyclitis Pars planitis Vitritis Chorioiditis Pigmentepithelitis AMPPPE Retinal vasculitis Endophthalmitis Neuro- ophthalmic manifestations Optic neuropathy Optic neuritis Ischemic neuropathy Optic atrophy Papilledema Pseudotumor cerebri Leber's neuroretinitis Cranial nerve palsy Facial nerve palsy Oculomotor palsy ( III, IV, VI) Pupillary disorders Argyll- Robertson pupil Horner's syndrome Organic manifestation Dermatologic Multiple erythema Neurologic Meningitis Radiculoneuritis Cranial neuritis Cardiac Myocarditis Pericarditis Atrioventricular block Rheumatologic Monoarthritis Oligoarthritis IgG: increasing IgM: high Data from Refs. 5, 9, and 10. AMPPPE, acute multifocal posterior placoid pigment epithiopathy. thalmitis following an insect bite causing erythema migrans. Lensectomy and vitrectomy were performed, and Lyme spirochetes were found in the vitreous specimens. Neuro- ophthalmic Manifestations Optic Neuropathy. Optic neuritis. To date, there are only a few reports of optic neuritis associated with borreliosis ( 1,7,11,17,22,24,26,44,45). Winward and associates ( 7) observed a case of bilateral optic neuritis and mild vitritis. In these patients, central scotoma and afferent pupillary defect were present, as well as other neurologic manifestations. Anterior ischemic optic neuropathy. A case of ischemic optic neuropathy secondary to Lyme disease with an inferior altitudinal field defect has been reported by Schechter ( 47). Pizzarello and coworkers ( 46) described another case of ischemic neuropathy following a tick bite causing erythema migrans. Temporal artery specimens showed the typical appearance of giant cell arteritis, but a silver stain suggested Borrelia spirochetes within the multinucleated giant cells and ceftriaxone therapy led to a marked improvement of visual acuity. Other cases have been described in the literature ( 29,32,46,47). Optic atrophy. Optic neuritis, ischemic neuropathy, and chronic papilledema in pseudotumor cerebri may each be responsible for optic disc atrophy ( 14,17,25,32,43,48) in patients with chronic Lyme borreliosis. Bertuch and colleagues ( 49) described a case of progressive optic disc pallor following a presumed Lyme disease without previously observed optic nerve disorders. Papilledema. Optic disc edema may result from various causes ( 1,14,17,22,28,33,43,45,50). Only a minority of patients with Lyme meningitis develop disc edema. The latter leads to blurred vision and is not usually associated with elevated intracranial pressure ( 35). Optic perineuritis. An optic perineuritis is probably the reason for disc swelling in the cases described by Kauffmann and colleagues ( 18), Reik and colleagues ( 14), Jacobson and Frens ( 50), and Farris and Webb ( 17). Pseudotumor cerebri. Lyme disease- associated pseudotumor cerebri with increased cerebrospinal fluid pressure has been reported in several cases ( 7,45,50,51). Leber's stellate neuroretinitis. Leber's stellate neuroretinitis is caused by vasculitis of the optic nerve head, causing distinct disc edema, venous congestion, and star- shaped lipoid exudation. It has been reported in viral diseases and neurolues ( 52). Recently, a few cases of this disorder in Lyme borreliosis have also been observed ( 1,43,45,52, 53). Cranial neuropathy. Facial nerve palsy. Facial nerve palsy, occasionally associated with keratitis, is the most common cranial neuropathy, occurring / Neuw- Ophthalmol, Vol. 14, No. 1, 1994 18 }. BERGLOFF ET AL. in approximately 50% of patients with Lyme meningitis ( 7,11,14,22,28,30,45,48,54- 57). Sometimes it can be seen as an isolated finding, although multiple recurrences have also been observed ( 7). Oculomotor palsy. Cranial neuropathy with oculomotor, trochlear, and abducens nerve palsies have been reported ( 7,9,11,12,14,22,37,45,56- 60). Diplopia is the typical ocular complaint in this context. These palsies may occur individually or in combination with other neurologic abnormalities. Lyme disease has been reported in children suffering from late- onset strabismus and diplopia ( 58,59). Pupillary Disorders. In the literature, there are only anecdotal reports about the association of pupillary dysfunction and Lyme disease. Argyll- Robertson pupil has been described in the report of Reik and coworkers ( 14) in 1986. This disorder is also common in neurolues. Another case with reversible Horner's syndrome has been observed by Glauser and coworkers ( 61). Ophthalmic Manifestations in Stage III See Table 3. Conjunctivitis and Episcleritis Zaidman ( 64) observed a case of chronic Lyme borreliosis with tarsoconjunctival scarring, sym-blepharon, and episcleritis. These manifestations are common in autoimmunologic eye diseases ( 22, 62,63). Thus, an immune- pathogenesis can also be considered in this case of late Lyme borreliosis. Keratitis Interstitial Keratitis. Interstitial keratitis in chronic spirochetal infections, for example, Treponema pallidum, is well known. In Lyme disease, several cases with scattered hazy infiltrates of the deep and superficial stroma have been observed ( 1,26,45,49,62,63,65- 69). Only one patient, however, exhibited corneal neovascularization, unlike the typical syphilitic keratitis parenchyma-tosa with early stromal vascularization ( 18,65). Interestingly, these cases of Lyme disease associated interstitial keratitis responded to local steroids, but not to antibiotic therapy, suggesting an immuno-pathologic origin ( 65). Peripheral Ulcerative Keratitis. A patient with peripheral ulceration secondary to Lyme disease has been presented ( 70). It is noteworthy that this manifestation is commonly seen in autoimmune diseases. Orbital Myositis A single case of orbital myositis has been described in the literature: a 5- year- old girl with typical manifestations of late Lyme borreliosis. This child developed unilateral orbital pain, proptosis, and diplopia. Computed tomography scans disclosed myositis of the medial and inferior rectus muscle and haziness of the retrobulbar fat. Complete resolution was seen after corticoid therapy ( 6). Neuro- ophthalmic Manifestations The typical central nervous system manifestation ( 9,11,14,43,48) in chronic borreliosis is a progressive encephalomyelitis with fatigue, dementia, and multiple cranial nerve palsies, as well as cerebellar and extrapyramidal defects and recurrent strokes. These disorders are thought to be caused by occlusive cerebral vasculitis ( 1). Magnetic resonance imaging ( MRI) shows multiple paraventricular and subcortical demyelinating lesions ( 1,14,17,43,45) similar to these seen in multiple sclerosis. CONCLUSION AND SUMMARY Ophthalmic manifestations of Lyme borreliosis are common and can mimic features of other systemic disorders. A variety of ocular disorders is found in each stage of Lyme disease. The growing awareness of Borrelia burgdorferi infections has cer- TABLE 3. Stage III (> 1 year) Ocular symptoms Keratitis Interstitial keratitis Peripheral ulcerative keratitis Episcleritis Myositis Neuro- ophthalmic manifestations Optic neuritis Ocular nerve palsies Visual field defects Nystagmus Systemic symptoms Organic manifestation Dermatologic Acrodermatitis chronica atrophicans Neurologic Progressive encephalomyelitis Rheumatologic Oligo arthritis Chronic- erosive arthritis Routine serology IgG: high IgM: low Data from Refs. 5, 9, and 10. I Neuw- Ophthttlmol, Vol. 14, No. 1, 1994 MANIFESTATIONS IN LYME BORRELIOSIS 19 tainly contributed to improved diagnosis, but there are still diagnostic difficulties. Especially in cases with uveitis, optic neuritis, or oculomotor nerve palsies, one has to consider Borrelia burgdorferi as a possible causal agent ( 7). It is advisable to investigate the possible history of tick bites, erythema migrans, and disease such as arthritis, but tick bite history may be negative in 30- 40% of cases. Serologic tests for confirmation of a clinical diagnosis of Lyme disease are helpful. A negative result in any clinical situation does not exclude this diagnosis. According to the test used, Lyme bor-reliosis may be seronegative in up to 50% of cases ( 32,71). In cases with neuro- ophthalmic involvement, an examination of the cerebrospinal fluid is recommended, although serologic testing may show negative results ( 59). However, rigorous criteria should be applied in order to avoid an overdiagnosis of the ocular manifestations of Lyme disease ( 9). Serologic investigations for Borrelia antibodies may be helpful, but one must be aware of the fact that, in endemic areas, positive IgG titers may be an occasional coincidence. The Centers for Disease Control proposed the definition of Lyme disease, as shown in Table 4 ( 9). In early Lyme disease oral antibiotic therapy shortens the duration of systemic symptoms and prevents development of delayed disease in most patients. The specific recommendations for antibiotic therapy have changed during the past few years, but treatment failures have occurred with every regimen. Oral tetracycline or penicillin are the current recommended drugs in stage I of Lyme disease. In later stages parenteral antibiotics, as penicillin or cephalosporin, are required ( 9,15,17, 32). The use of corticosteroids in chronic borrelio-sis is controversial. Steroids apparently have been helpful in treating keratitis, myositis, or certain neurologic symptoms in stage III of Lyme disease ( 6,15,49,65,68). However, one should always be cautious when using steroids with Lyme borreliosis, since they may cause severe exacerbation of all the clinical symptoms. Once Borrelia burgdorferi in- TABLE 4. Diagnostic criteria for Lyme disease Area Criteria Endemic 1. Erythema migrans with exposure not more than 30 days prior to onset 2. Involvement of one organ system0 and positive antibody test Nonendemic 1. Erythema migrans with positive antibody test 2. Erythema migrans with involvement of two organ systems3 Data from Ref. 9. " Musculoskeletal, neurologic, cardiac. fection is diagnosed, steroids should only be used together with high doses of intravenous antibiotics, even in late stages of Lyme disease. The postulated pathophysiologic mechanism of disease is direct bacterial invasion of the tissue and subsequent immunologic reactions resulting in vascular occlusions in chronic stages of the disease ( 10,26,65). Borrelia burgdorferi has been cultured from blood, from cerebrospinal fluid, and directly from brain parenchyma ( 10,16,45), but it has also been identified histologically in the retina and in the vitreous humor ( 17- 19). In chronic Lyme bor-reliosis, immunologic reactions are thought to play a predominant role ( 26,65). The nature of the underlying mechanisms, however, has not so far been elucidated. The increasing number of reports of Lyme disease- associated ocular disorders should alert ophthalmologists to Borrelia burgdorferi as a possible causal agent. Serologic investigations for Lyme disease antibodies are recommended in cases with ocular inflammatory diseases, optic neuropathies, or cranial nerve palsies. 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