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Neurosyphilis in HIV

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Neurosyphilis in HIV 1 of 16 Neurosyphilis in HIV Emily Hobbs 1, Jaime H Vera 1,2 , Michael Marks 3, Andrew W Barritt 1,4 , Basil H Ridha 1,4, and David Lawrence 2,3* 1 Affiliation 1; Brighton and Sussex Medical School University of Sussex, Falmer, Brighton, BN1 9PX, United Kingdom 2 Affiliation 2; Lawson Unit, Royal Sussex County Hospital, Eastern Road, Brighton, BN2 5BE, United Kingdom 3 Affiliation 3; Clinical Research Department, The London School of Hygiene and Tropical Medicine, Keppel Street, London, WC1E 7HT, United Kingdom 4 Affiliation 4; Hurstwood Park Neurological Centre, Haywards Heath, Sussex, RH16 4EX. * Correspondence: [email protected]; Tel.: +267 724 64 834 Keywords: Neurosyphilis, syphilis, HIV Word count: 4072 2 of 16 Abstract: Syphilis is a resurgent sexually transmitted infection in the UK which is disproportionately diagnosed in patients living with HIV, particularly men who have sex with men. Evidence exists to suggest that syphilis presents differently in patients with HIV, particularly in those with severe immunosuppression. Progression to neurosyphilis is more common in HIV co-infection and can be asymptomatic, often for several years. Symptoms of neurosyphilis vary but can include meningitis, meningovascular disease, general paresis and tabes dorsalis. Debate exists surrounding in which circumstances to perform a lumbar puncture and the current gold standard diagnostics have inadequate sensitivity. We recommend a pragmatic approach to lumbar punctures, interpretation of investigations, and when to consider treatment with a neuropenetrative antibiotic regimen. THE CHANGING FACE OF SYPHILIS Syphilis, caused by the spirochaete bacterium Treponema pallidum, has seen a resurgence in high-income countries in recent years, particularly among men who have sex with men(1). The widespread availability of penicillin in the United States and other industrialised countries following World War Two resulted in rates of syphilis falling from 76 per 100,000 population in 1945 to 4 per 100,000 in 1955-57. After this period syphilis became concentrated within men who have sex with men and incidence surged during the 1980s HIV/AIDS epidemic(1). In response to the fear induced by the epidemic, changes in sexual behaviour caused another decline until recently where rates have risen rapidly again(1, 2) . In the United States during 2014-2015 syphilis occurred in 7.5 cases per 100,000, the highest rate since 1994(3). Similar trends were seen in England where in 2016 the number of cases was 5920 (Figure 1)(4), 12% higher than the previous year and the highest number of new diagnoses since 1949, with 80.9% of cases reported in men who have sex with men(2). SYPHILIS INFECTION Syphilis infection involves a number of stages. Primary syphilis classically presents 9-90 days after infection with a single, non-tender genital ulcer called a chancre which represents the first site of T.pallidum invasion. If untreated, primary infection progresses to secondary syphilis, typically 12 weeks, but sometimes up to 12 months after initial infection. The classic presentation of secondary syphilis is a rash which typically involves the trunk, may involve the hands or feet and may be accompanied by condylomata lata, wart-like lesions around the anogenital region. Latent syphilis results when both primary and secondary syphilis are not treated and is defined by serological proof of infection but no symptoms. It is divided into early and late latent syphilis, with early latent syphilis infectious and late latent syphilis, defined in the UK as more than two years after infection, found to generally be non-infectious (5, 6). Syphilis will progress to tertiary disease in one third of patients without treatment roughly 20- 40 years after primary infection(5). Tertiary syphilis involves a severe and self-destructive 3 of 16 immune response to a persistent low level burden of T. pallidum (5). This can present as cardiovascular syphilis, gummatous syphilis, late benign syphilis or neurosyphilis(6). It is important to emphasise that neurological symptoms can occur during any phase of infection and therefore neurosyphilis should only be considered tertiary when presenting in the late- latent period(5). Primary, secondary and early latent syphilis are collectively grouped together as early syphilis and late latent and tertiary syphilis are grouped together as late syphilis. NEUROSYPHILIS Neurosyphilis is a broad term used to describe the direct invasion of T pallidum into the nervous system and can affect the brain, spinal cord and peripheral nerves(7). Approximately 25-40% of patients will have ‘neuroinvasion’ at some point, typically during the primary or secondary stage of infection, but the majority will spontaneously clear the infection from the cerebrospinal fluid (CSF) without requiring treatment for neurosyphilis and potentially without having any symptoms(8). In patients whose immune system is unable to clear the infection, neurosyphilis will occur and this can also present with or without symptoms, the latter form known as asymptomatic neurosyphilis(7). There exists great debate around the topic of asymptomatic neurosyphilis which is discussed below. Syphilis is often referred to as ‘the great imitator’ and it can present in countless ways. The clinical manifestations of neurosyphilis are similarly varied and patients may remain asymptomatic for years. Levels of central neurological involvement can be classified into meningeal, vascular or parenchymatous forms with direct invasion of T. pallidum possible at each of these sites (9). Meningeal and vascular neurosyphilis are inflammatory processes which frequently coexist (meningovascular neurosyphilis), particularly in the early years of infection(10). Meningeal involvement can present as aseptic meningitis with symptoms such as headache, photophobia and neck stiffness and can lead to complications such as cranial nerve palsies(9). Vascular syphilis can affect the arterial supply of the brain or spinal cord resulting in ischaemic stroke and, depending on the arterial territory involved, can cause different neurological deficits. Neurosyphilis should therefore always be considered as a differential diagnosis in any patient with ischaemic stroke of unknown aetiology, particularly in young people(9). Parenchymal neurosyphilis is neurodegenerative in nature and can manifest as general paresis characterised by memory deficit, emotional lability, psychosis or tabes dorsalis (also known as syphilitic myelopathy) in which patients may develop sensory ataxia and neuropathic pain in the lower limbs(11, 12). Parenchymal changes tend to arise years to decades after initial infection and due to the widespread availability and prescribing of penicillin are now extremely rare(11, 13). A fourth, distinct and rare form of central neurosyphilis can emerge in gummatous syphilis which causes space occupying lesions which may result in seizures, focal neurological signs, raised intracranial pressure or progressive paraparesis or quadriparesis(9). Involvement of the peripheral nervous system is not the focus 4 of 16 of this review and is less common but can include polyradiculopathy and peripheral neuropathy(14). THE SYNERGISTIC RELATIONSHIP BETWEEN HIV AND SYPHILIS HIV and syphilis affect similar patient groups and in 2002 the United States Center for Disease and Control Prevention (CDC) reported the incidence of syphilis to be 77 times greater in HIV infected individuals than that of the general population(15). This is of particular significance because HIV and syphilis have a synergistic relationship wherein syphilis can increase the risk of HIV transmission and acquisition whilst HIV can affect the presentation, diagnosis, progression and treatment response of syphilis(16). A large body of the evidence related to this is presented in the context of advanced HIV and might not apply to those with CD4 counts ≥ 350 cells/µL and/or a suppressed HIV viral load. In terms of HIV acquisition , syphilis causes transient immunosuppression and can weaken the host response to HIV, increasing the likelihood of exposure leading to HIV infection. In addition to this, chancres are particularly vulnerable, well vascularised sites for HIV to enter the bloodstream and establish primary infection(17, 18). The impact of HIV on syphilis is explained by the immunodeficiency caused by HIV and the presentation of syphilis may be more severe or atypical, particularly in the severely immunosuppressed. These individuals are more likely to develop multiple, deeper or larger chancres and can have primary and secondary infection overlap(19). This trend continues in the context of neurosyphilis: A review of syphilis cases in Los Angeles between 2001 and 2004 showed a 2.1% incidence of neurosyphilis among those infected with HIV compared to 0.6% among those without HIV(20). The likelihood of developing neurosyphilis has been linked to the degree of immunosuppression caused by HIV with it being suggested that patients with a CD4 count of ≤ 350 cells/µL have a 3-fold increase in neurological involvement(21). ASYMPTOMATIC NEUROSYPHILIS Asymptomatic neurosyphilis is a topic of significant debate and scientific uncertainty. Concerns arose from studies which reported a greater level of neurocognitive impairment in HIV positive patients with previous early-syphilis but no diagnosis of neurosyphilis who were treated with standard Benzathine Penicillin G, which does not cross the blood-brain barrier, when compared to those without previous syphilis. Unfortunately
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