Retroviral infections and AIDS

Introduction

Retroviruses are a group of RNA viruses which derive their name from their unusual mode of replication. They contain the enzyme reverse-transcriptase which synthesizes DNA from the viral RNA. The DNA is then integrated into the host genome and serves as the template for the synthesis of viral genomic RNA and messenger RNA. Retroviruses had been known for many years to cause a number of diseases in animals. However, it was only in 1978 that the first retrovirus associated with human disease was identified (HTLVI, the human T-lymphocytotropic virus) (Gallo 1984[1]).

The acquired immune deficiency syndrome (AIDS) was first described as a clinical entity in 1981 and has since emerged as a major worldwide problem. Within 2 years of the description of AIDS, a new group of retroviruses was implicated as the cause of the disorder. In the past few years there has been an explosion in knowledge of the biology of the human retroviruses, and their role in AIDS and other diseases (Gallo 1987[2]). Four different retroviruses are now known to be associated with human disease (Table 22.18)

Table 22.18

, although a number of other human retroviruses are also known to exist. HTLV 1, the first human T lymphotropic virus to be identified, is causally associated with adult T -cell leukaemia and tropical spastic paraparesis. HTLV II has been isolated from patients with hairy cell leukaemia and may cause a myelopathy (Murphy 1993[3]). The human immunodeficiency viruses, HIV 1 (previously termed HTLV III) and HIV 2 are the causative agents of AIDS (Dalgleish & Weiss 1987[4]).

Tropical spastic paraparesis

Physicians working in tropical and sub-tropical countries have for many years been familiar with a syndrome of slowly progressive spastic paraparesis, without evidence of spinal cord compression or motor neuron involvement. Cases of this chronic progressive myelopathy, which occurs in adults and infrequently in teenagers, occur in geographical clusters throughout Africa, India, Central America, South America and the Caribbean Islands (Roman et al 1985[5]). In 1985, Gessain et al[6] reported an association between HTLV 1, the retrovirus initially associated with adult T -cell leukaemia, and tropical spastic paraparesis in Martinique (French West Indies). The association between HTLV 1 and progressive myelopathy has now been confirmed in patients from Japan, Colombia, the Seychelles and Jamaica, and it has been suggested that the condition be called 'HTLV 1-associated myelopathy'. More recently, additional evidence to support the pathogenic role of HTLV 1 infection in progressive neurological damage has emerged. The virus has been isolated from the CSF mono-nuclear cells of infected patients, and viral nucleic acid sequences have been identified in their CSF. Furthermore, intrathecal synthesis of antibodies against HTLV 1 has been demonstrated, and the oligoclonal bands present in the CSF of affected patients have been shown to react with viral antigens (Roman 1987[7], Brew & Price 1988[8], Bhagavati et al 1988[9]).

Despite the clear association of HTLV 1 infection with myelopathy, the underlying pathogenic mechanisms remain to be elucidated. Seropositivity to HTLV 1 is common in populations in southern Japan and a variety of equatorial regions. However, the two diseases associated with this virus, progressive myelopathy and adult T -cell leukaemia, are extremely rare. The reasons why the virus only causes symptomatic disease in a small proportion of affected patients is unknown. However, the linking of retroviral infection with progressive neurological diseases raises the exciting possibility that other neurological conditions may ultimately be explained on the basis of chronic viral infections.

CNS disorder in HIV infection and AIDS

Children acquire HIV either perinatally from an infected mother or through blood products obtained from an infected donor. While the number of children infected by transfusions has declined dramatically following the introduction of routine testing of blood products, the number of perinatally infected children is increasing in parallel with the number of infected adults (Chin 1990[10]). Although the incidence of HIV infection in developed countries is greatest in high-risk population groups (intravenous drug users, prostitutes and male homosexuals), the infection has now spread to the general population, and increased numbers of patients are being recognized in whom no clear risk factors can be identified. In Africa, where the incidence in some countries is as high as 30% of the population (Shao 1994), the disorder is predominantly spread heterosexually and by perinatal transmission.

The rate of transmission of HIV infection from an infected mother to her infant is influenced by a number of factors including the mother's clinical, immunological and viral status, the infant's gestational age at delivery, the mode of delivery (e.g. Caesarean section versus vaginal delivery) and whether the infant is breast fed or bottle fed. In Europe, the transmission rate is in the region of 15% (European Collaborative Study 1992[11]), but in the USA and Africa, rates appear to be higher. The HIV infection status is difficult to establish in the first few months of life as all these infants will have transplacentally acquired maternal antibodies against the virus. The majority subsequently become seronegative and have no evidence of infection on follow-up, but this seroreversion can take up to 18 months to occur. Newer techniques which specifically demonstrate the presence of virus (HIV culture and PCR) are becoming available. The sensitivity and specificity of these are such that testing of two or three samples from the infant should establish the infection status by about 6 months of age.

The clinical features of HIV infection are very varied and overlap those of many of the common childhood illnesses (Pahwa 1988). The infection may remain asymptomatic for a prolonged period of time or may follow a rapid progressive course leading to death in the first year of life. Infants frequently present with acute life-threatening illness, especially pneumocystis carinii pneumonia, whereas older children may present with non-specific symptoms: failure to thrive, lymphadenopathy, hepatosplenomegaly, chronic diarrhoea, frequent upper respiratory tract infections,repeated oral candidiasis, skin rashes and developmental delay. Pulmonary manifestations are present in a high proportion of cases and include lymphoid interstitial pneu-monitis, repeated episodes of pneumonia and opportunistic infections, especially Pneumocystis carinii pneumonia. Unlike adults, children with HIV frequently have repeated episodes of bacterial infections caused by common childhood pathogens such as pneumococcus (Pahwa 1988, Shannon & Ammann 1985[12, 13]).

Neurological involvement in the form of encephalopathy is a common feature of HIV infection in children (Epstein et al 1986, Belman et al 1985[14, 15]). Other forms of nervous system involvement are rare in children but seizures, mye-lopathy (Mintz 1989a[16]) and peripheral neuropathy (Raphael 1991) have been described. In most cases of encephalopathy, this is believed to be due to a direct effect of the virus on the central nervous system, but the brain may also be invaded by secondary opportunistic infections. The differential diagnosis of CNS dysfunction in HIV infected children is therefore a difficult problem which requires careful clinical assessment, the use of CT or MRI scanning and help from a microbiological laboratory familiar with techniques to identify opportunistic pathogens. The causes of CNS dysfunction in children with AIDS are listed in Table 22.19

File:Bretts chapter table 22.19

Table 22.19

.

HIV encephalopathy usually occurs after the onset of other severe symptoms, but has been described as the presenting clinical feature (Scott 1989[17]). In the infant it presents with developmental delay, cognitive defects (especially in expressive language) and motor problems (especially spastic diplegia). In the toddler it presents with loss of skills and regression. In older children, after a period of normal development, it may present as behavioural abnormalities. It is probable that the full clinical spectrum has yet to be described and increasingly diverse neurological symptoms will be observed in HIV infected children. The encephalopathy may be static, slowly or rapidly progressive. Early diagnosis is best made on longitudinal neuropsychological testing. Later brisk leg reflexes, generalized spasticity, bulbar paralysis and microcephally may develop. Neuroradiological investigations may reveal abnormalities, especially in advanced cases. Cerebral atrophy with ventricular enlargement and widening of the sulci (due to shrinking of the white matter) is seen along with calcification in the basal ganglia, a finding which is said to be pathonemonic ( Belman 1986, Epstein 1985[18, 19]). CSF may be normal or may show increased protein and a lymphocytic pleocytosis. The value of performing a lumbar puncture is therefore to help in excluding other causes of encephalopathy.

Distinctive histopathological findings are seen in the brains of children with HIV encephalopathy (Sharer 1986). Vascular and perivascular calcification frequently accompanied by an inflammatory reaction are seen in the basal ganglia and cerebral white matter. This inflammatory process can also extend into the leptomeninges. White matter pallor is seen in advanced cases. Inflammatory infiltrates consisting of microglia, mononuclear cells, astro-cytes, lymphocytes and multinucleate-giant-cells are observed throughout the CNS, but are most frequently seen within the basal ganglia and spinal cord. Neuronal loss is not characteristically seen.

The neuropathogenesis of the widespread histological damage remains unclear. It is believed that HIV gains access to the central nervous system through migration of infected monocytes and macrophages across the blood-brain barrier, and there is data to suggest that such invasion occurs early in the course of HIV infection, long before the onset of CNS symptoms (Resnick 1988[20], Hollander 1987[21]). The virus can be demonstrated within or closely associated with multinucleate-giant-cells and microglial cells by immunohistochemical staining and in situ hybridization techniques (Michaels 1988, Koenig 1986, Wiley 1986[22, 23, 24]), but there is no direct evidence for the occurrence of infection within neurones. The mechanism of tissue damage may be due to a combination of viral factors and host mediated factors. In vitro studies have suggested that HIV envelope glycoprotein GP 120 is toxic to neurones by promoting calcium influx (Brenneman 1988), but this observation only appears to occur if monocytes and glial cells are also present. This toxic effect can be blocked by calcium channel blockers such as nifedepine (Dreyer 1990) and by antagonists of the N-methyl-D-aspartate (NMDA) receptor channel complex (Lipton 1991[25]). Activation of the NMDA receptor has been implicated in the pathogenesis of other neuropathological processes leading to neuronal death (Lipton 1992[26]) and may act as a final common pathway in HIV encephalopathy. Indirect mechanisms mediating tissue damage are suggested such as toxic effects of cytokines produced in the inflammatory response. Tumour necrosis factor alpha (TNF alpha) is one such potential cytotoxic mediator capable of inducing myelin damage in vitro (Selmaj 1988[27]), and elevated circulating levels of TNF alpha have been reported in children with progressive HIV encephalopathy (Mintz 1989b[28]).

Management of HIV encephalopathy depends upon establishing the diagnosis of excluding opportunistic infections. Symptomatic and neuroradiological improvement is usually seen in response to zidovudine (Pizzo 1988[29], DeCarli 1991[30]). However, the duration for which this improvement is sustained is unpredictable and often spans only a few months. Data on CNS penetration and effectiveness of newer anti-retroviral drugs in HIV encephalopathy are lacking, but their usefulness may be limited because of poor CNS penetration (Pizzo 1990[31]). As ence-phalopathic symptoms progress, multidisciplinary input is required to try to minimize the effects of the child's disabilities.

Opportunistic infections of the CNS occur less commonly in HIV infected children than in adults, but must be searched for and excluded in every case as some are potentially treatable. Bacterial meningitis caused by the usual childhood pathogens may be the presenting feature of AIDS. Meningitis due to less common pathogens, particularly Salmonella, should alert the clinician to the possibility of underlying HIV infection ( Bernstein et al 1985, Kranski et al 1988[32, 33]).

CNS toxoplasmosis is less common in HIV infected children than in adults with the disease. It presents either as a subacute meningoencephalitis or as a space-occupying lesion. Non-specific features such as headache, lethargy and drowsiness are followed by the development of focal neurological signs (Loft & Remington 1988[34]). The CSF protein is usually elevated, often with a mononuclear pleo-cytosis. CSF glucose concentrations are normal or only slightly depressed. CT scanning reveals contrast-enhancing lesions with surrounding oedema and evidence of a mass effect. The lesions are most common in the cerebral hemispheres and basal ganglia. Toxoplasma serology may be unreliable in confirming the diagnosis, as the immune defect may prevent development of a normal antibody response. Differentiation between cerebral lymphoma can be extremely difficult. A definite diagnosis can be made by brain biopsy, in which toxoplasma cysts or tachyzoites are seen at the edges of necrotic lesions. However, lesions may be inaccessible or biopsy considered too hazardous, in which case a trial of toxoplasma treatment should be commenced. Treatment with pyrimethamine and sulphadiazine may result in considerable improvement, but prolonged treatment is required as recurrence often occurs on discontinuation of treatment (Holliman 1988[35]).

Cryptococcal meningitis has emerged as a common cause of meningitis in adults with AIDS, and occasionally occurs in children. The disease presents as a subacute or chronic granulomatous meningitis. Initial symptoms are of headache, lethargy and meningeal irritation. Later, signs of raised intracranial pressure and papilloedema occur. The CSF usually shows a pleocytosis with elevated CSF protein and a depressed glucose concentration. The diagnosis is confirmed by visualization of the organisms by India ink staining and culture. Cryptococcal antigen tests are probably the most sensitive method for diagnosis, but even this may be negative. In suspected cases, repeated CSF examination should be undertaken. Treatment with amphotericin B and 5-flucytosine results in considerable improvement in the condition, but relapses are common on stopping treatment (Pippard et al 1986, Dismukes 1988) and long-term prophylaxis with fluconazole is recommended (Powderly 1992[36]).

Other uncommon opportunistic CNS infections include atypical mycobacterial infection, Nocardia, CMV and herpesvirus infections (Curless et al 1987[37]). Progressive multifocal leuco-encephalopathy, caused by a papovavirus QC virus), is common in adults but appears to be rare in children. Malignancy, especially lymphoma, must be considered in the differential diagnosis of CNS lesions in children with AIDS (Katz et al 1986[38]). Cerebral vascular accidents (CVAs), especially when the child has HIV related thrombocytopaenia, are also seen.

Progressive multifocal leuco-encephalopathy

Progressive multifocal leuco-encephalopathy (PMLE) was first described in immunosuppressed patients 40 years ago, and is characterized by multiple progressively-evolving demyelinating lesions in the brain (Richardson 1961[39]). Originally thought to be an extremely rare complication of illnesses such as leukaemia and lymphomas, it has now emerged as an important and relatively common disease process in adults with AIDS and other immunological deficiency states (Richardson 1988). The disease occasionally occurs in children with advanced HIV and has been reported in an immunocompetent child (Blake 1992). The disorder presents with focal or generalized limb weakness, visual field defects, ataxia and dementia. CT scanning or nuclear magnetic resonance studies show multifocal, progressively enlarging lesions of the cerebral fibre systems. In 1965 viral particles were visualized in the pathological lesions on electron microscopy, and it has subsequently been established that the disorder is due to a papovavirus, now called JC virus (Houff et al 1988[40]). Seroepidemiological studies indicate that infection with JC virus is ubiquitous among adults all over the world. In the vast majority of the infected population, the virus produces no disease and remains dormant throughout life. However, under conditions of chronic immunosuppression it maybecome pathogenic and produce the picture of PMLE. The disease is invariably fatal and has not so far been shown to respond convincingly to any form of treatment. With increasing numbers of immunosuppressed children and especially children with AIDS, PMLE is likely to become a more frequent paediatric problem (Berger et al 1987[41]).

The prion diseases

The term 'prion' was introduced to describe a class of infectious agents which affect the CNS and are distinct from viruses. The diseases caused by these agents have previously been called the transmissible spongiform encephalopathies, and include scrapie in sheep, transmissible mink encephalopathy and the human diseases Kuru, Creutzfeldt-Jakob disease and Gertsmann-Straussler syndrome (Prusiner 1987[42]). All the prion diseases are confined to the CNS, and have prolonged incubation periods prior to the development of a progressive and ultimately fatal neurological illness. Pathologically they are associated with vacuolation of neurons and reactive astrocytosis and took their previous name from the striking spongy degeneration seen in the cerebral cortical grey matter. A major advance in the identification of the causative agents came from the detection and subsequent purification of protein fibrils seen in the brains of animals with scrapie (Prusiner 1982). Transmission in animals under laboratory conditions confirmed the infectivity of prions. Attempts to identify specific nucleic acid within highly purified preparations of prions have been unrewarding (Meyer 1991[43]). These scrapie-associated fibrils are composed of a protein, denoted as PrPs , which is the major component of the infectious agent. Antibodies against the protein have been used to show that. similar proteins are present in the amyloid plaques found in the brains of patients dying of Creutzfeldt-Jakob disease and Kuru (Merz et al 1984[44]). The finding of prion protein mRNA in uninfected as well as scrapie infected tissues led to the discovery of the normal prion protein isoform, denoted as PrPc (Chesebro 1985[45]). The function of PrPc is unknown. Studies on the structure of PrP c and PrPs have been unsuccessful in defining a post-translational chemical modification that distinguishes one isoform from the other. PrPs~ is synthesized from PrPc by an unknown post-translational process (Borchelt 1992[46]). Cloning the prior protein gene led to the discovery of a point mutation for humans with familial CJD and established that prion diseases are both genetic and infectious in humans.

Kuru

Kuru is a fatal progressive neurological disease confined to one ethnic group of New Guinea highland tribesmen. The illness presents with loss of coordination, slurred speech and clumsiness, and progresses to severe ataxia, inability to swallow and cranial nerve and pyramidal tract dysfunction. Death usually occurs 6-12 months after the onset of symptoms. Women are affected more often than men. The meticulous epidemiological studies undertaken by Gadjusek implicated the practice of ritual cannibalism in the transmission of the disease. Women appeared to be infected during the culinary preparation of infected brain tissue. Since the practice of cannibalism has ceased, the incidence of the disease has declined dramatically, and the disorder is now confined to adults infected several decades ago (Gajdusek & Vigas 1959, Gajdusek 1977[47, 48]).

Creutzfeldt-Jakob disease

This is a progressive dementing illness characterized by profound dementia, loss of all intellectual functions and sometimes cerebellar and visual defects. Neuropathological studies reveal similar changes to those in kuru and scrapie, with vacuolation of the grey matter, astrocytosis and the presence of characteristic scrapie-associated fibrils (Masters & Richardson 1978). No epidemiological link between scrapie and Creutzfeldt-Jakob disease has been demonstrated. The disease has been transmitted to primates by injection of infected brain. Although normally a disease of the elderly, of importance in paediatric practice is the outbreak of Creutzfeldt Jakob disease in patients from as young as 10 years old who had received human growth hormone prepared from human pituitary glands which had been contaminated with prions from patients with CJD (Fradkin 1991[49], Buchanan 1991[50], Gibbs et al 1985[51]). Considering the possible long incubation period, this rare disease could be seen in many more recipients of human growth hormone derived from human pituitary. Transmission has also occurred through corneal transplantation, contaminated EEG electrode implantation and by inadequate sterilization of surgical instruments. The infectious agent appears to be highly resistant to many sterilizing and inactivating procedures.

More recently, the epidemic in the United Kingdom of bovine spongiform encephalopathy (BSE), which may have arisen in cattle eating bone meal contaminated with scrapie prions, has generated fears of transmission of a similar encephalopathy to humans eating BSE infected beef. No epidemiological link between BSE and CJD is yet proven, but reports of a new variant of the disorder in the UK are alarming (Will et al 1996[52]). This variant form occurs at a younger age, including teenage, presents with personality changes, mental disturbance and dysaesthesia and progresses to ataxia and dementia. The cases were diagnosed by brain biopsy or at post mortem and showed the presence of PrP plaques surrounded by a zone of spongiform change, a feature not seen in sporadic CJD.

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