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1 Table 16.3 Examples of s in humans Microorganism Site of persistence Infectiousness of microorganism Viruses Consequence Herpes simplex Dorsal root ganglia Activation, cold sore + Salivary glands + Not known + Varicella-zoster Dorsal root ganglia Activation, zoster + Cytomegalovirus Lymphoid tissue Activation ± + Lymphoid tissue Lymphoid tumour Epithelium Nasopharyngeal carcinoma Salivary glands + Not known + Hepatitis B and C Liver (virus shed into blood) + Chronic hepatitis: liver cancer + Adenoviruses Lymphoid tissue None known + Polyomaviruses BK and Kidney Activation (pregnancy, + JC (humans) immunosuppression) T-cell leukaemia viruses Lymphoid and other tissues ± Late leukaemia, neurologic Paramyxovirus Brain ± Subacute sclerosing panencephalitis HIV Lymphocytes, macrophages + Chronic + Chlamydia Chlamydia trachomatis Conjunctiva + Chronic and blindness + Rickettsia Rickettsia prowazekii Lymph node? Activation + Bacteria Salmonella typhi Gall bladder + Intermittent shedding in urine, + Urinary tract faeces Mycobacterium Lung or lymph nodeless? Activation, (immunosuppression, + tuberculosis (macrophages?) old age) Treponema pallidum Disseminated ± Chronic Parasites Plasmodium vivax Liver? Activation, clinical malaria + Toxoplasma gondii Lymphoid tissue, muscle, ± Activation, neurological brain Trypanosoma cruzi Blood, macrophages ± Chronic Schistosome mansoni Gut + Chronic Eggs Filaria Lymphatics, lymph nodes + Chronic + Shedding to the exterior takes place either directly, for example via skin lesions, saliva or urine, or indirectly via the blood (hepatitis B, malaria). Shedding of microorganism to exterior Other examples include the production by Pseudomonas of an elastase that inactivates the C3b and C5a components of complement and hence tends to inhibit opsonic and other host defence functions of complement. Unfortunately, although the above phenomena look convincingly like microbial adaptations for upsetting host defences, it is not always easy to prove that this is the case. PERSISTENT INFECTIONS Persistent s represent a failure of host defences One way of looking at s ( Table 16.3 ) is to regard them as failures of host defences. Host defences are designed to control and spread and to eliminate the microbe from the body. The microbe may persist: in a flagrantly defiant infectious form, as with hepatitis B in the blood or the schistosome in the blood vessels of the alimentary tract or bladder in a form with low or partial infectivity, for instance adenoviruses in the tonsils and adenoids i n a m e t a b o l i c a l l y a l t e r e d s t a t e, s u c h a s M. tuberculosis in a completely non-infectious form, often without producing any microbial antigens. Latent virus s are classic examples of this type of persistence. In the case of HSV, viral DNA persists for many years, probably for life, in sensory neurones in the dorsal root ganglia. The molecular basis for viral latency has still not been elucidated. It involves special adaptations by the virus to the state of latency in the case of HSV and VZV, there is very limited transcription of viral RNA in infected neurones, known as latency-associated transcripts. The viral genome is not integrated with host DNA, and instead of being linear it is circular, and exists in free episomal form. 173
2 CHAPTER 16Parasite survival strategies and s elimination of microbe Infection type acute self-limited Examples influenza rotavirus whooping cough microbe persists in infectious form with continuous or intermittent shedding with shedding tapeworms reactivation with and shedding microbe persists in latent non-infectious form latent herpes simplex virus varicella-zoster virus reactivating tuberculosis malaria (P. vivax/ P. ovale) final microbe growth continues somes in privileged site slow following acute SSPE PML HIV (AIDS) HTLV1 (leukaemia) final continued slow slow (no acute stage) Creutzfeldt Jakob Figure Patterns of acute and s. For some microbes (e.g. CMV, tuberculosis), the distinction between persistence in infectious form and true latency is not clear. HTLV1, human T-cell leukaemia virus 1; PML, progressive multifocal leukoencephalopathy; SSPE, subacute sclerosing panencephalitis. Latent s can become patent Latent s are so-called because they can become patent. This is where they become of immense medical interest, and the legacy of latent herpesvirus s in humans is described in Chapter 26. Different patterns of s are illustrated in Figure 16.11, and they are important for four main reasons: 1. They can be reactivated. 2. T h e y a r e s o m e t i m e s a s s o c i a t e d w i t h c h r o n i c d i s e a s e, a s in the case of chronic hepatitis B s, subacute sclerosing panencephalitis following measles, and AIDS. 3. They are somes associated with cancers, such as hepatocellular carcinoma with hepatitis B virus, and Burkitt's lymphoma and nasopharyngeal carcinoma with EBV. 4. From the microbial viewpoint, they enable the infectious agent to persist in the host community ( Box 16.2 ). 174
3 Box 16.2 Lessons in Microbiology Persistence is of survival value for the microbe Persistence without any further shedding, as occurs in subacute sclerosing panencephalitis and progressive multifocal leukoencephalopathy (see Ch. 24 ), is of no survival value, but there are obvious advantages if the microbe is also shed, either continuously or intermittently. This is especially true when the host species consists of small isolated groups of individuals ( Fig ). Measles, for instance, is not normally a. It only infects humans, does not survive for long outside the body and has nowhere else to go (i.e. there is no animal reservoir). Without a continued supply of fresh susceptible humans, the virus could not maintain itself and would become extinct. There has to be, at all s, someone acutely infected with measles. From studies of island communities it is clear that you need a minimum of about humans to maintain measles without reintroduction from outside. In Palaeolithic s, when humans lived in small, isolated groups, measles could not have existed in its present form. In contrast, and latent s are admirably adapted for survival under these circumstances. VZV can maintain itself in a community of < 1000 individuals. Children get chickenpox, the virus persists in latent form in sensory neurones, and later in life the virus reactivates to cause shingles. By this, a new generation of susceptible individuals has appeared and the shingles vesicles provide a fresh source of virus. Serologic studies show that the viral s prevalent in small, completely isolated Indian communities in the Amazon basin are or latent (e.g. due to adenoviruses, polyomaviruses, papillomaviruses, herpesviruses) rather than non- (e.g. due to influenza, measles, poliovirus). The same principles apply to non-viral s. Those present in small communities are either /latent (typhoid, respiratory tuberculosis) or have an animal reservoir for maintenance of the microbe. non- microbe (e.g. measles) small community infected individuals large community microbe infects susceptibles microbe dies out unless re-introduced microbe infects susceptibles, spreads through community causing repeated outbreaks as fresh susceptibles appear microbe (e.g. varicella-zoster virus) small community microbe infects susceptibles microbe remains latent Figure Persistence is a microbial survival strategy. microbe reactivates, infects next generation of susceptibles Reactivation of latent s Reactivation is clinically important in immunosuppressed individuals Reactivation occurs in immunocompromised patients, and is of major clinical importance in those immunosuppressed as a result of chronic or (AIDS), tumours (leukaemias, lymphomas), or in those immunosuppressed by the physician following transplantation ( Table 16.4 ). Reactivation also occurs during naturally occurring periods of immunocompromise, the most important of these being pregnancy and old age. From the microbe's point of view, latency is an adaptation that allows reactivation with renewed growth and shedding of the infectious agent during these naturally occurring periods. Features of reactivation in herpesvirus s are described in Chapters 21 and 26. We still know very little about reactivation mechanisms at the molecular level, as might be expected in view of our ignorance about the latent state itself. Latency is often thought of as a period when the microbe is in deep sleep. However, recent experiments suggest it may be a more active state. For example, M. tuberculosis needs to make certain proteins to keep itself in a latent state. Other products called resuscitation promoting factors may be needed to wake up latent M. tuberculosis. It is useful to distinguish two stages in reactivation The first event (stage A) in reactivation ( Fig ), the resumption of viral activity in the latently infected cell, is the most mysterious stage. In the case of HSV, this can be triggered by sensory stimuli arriving in the neurone (from skin areas responding to sunlight) and also by certain fevers (i.e. during other s) or by hormonal influences. Little more than this is known. 175
4 CHAPTER 16Parasite survival strategies and s Table 16.4 Reactivation of s Circumstance Infectious agent Site of shedding Old age Varicella-zoster virus Skin vesicles Mycobacterium tuberculosis Lung Pregnancy Polyomaviruses (BK, JC) Urine Cytomegalovirus Cervix Herpes simplex virus 2 Cervix Saliva Leukaemias, lymphomas (e.g. Hodgkin's ) Varicella-zoster virus Skin vesicles Polyomavirus CNS (PML) a Post-transplant immunosuppression Herpes simplex virus Skin/mucosal lesions Varicella-zoster virus Skin vesicles Wart viruses Skin Cytomegaloviruses Viraemia, pneumonitis a Saliva Hepatitis B,C Blood Polyomavirus (BK) Urine HIV Pneumocystis jirovecii b Lung a Toxoplasma gondii CNS a Varicella-zoster virus Skin vesicles Herpes simplex virus Skin/mucosal lesions Mycobacterium tuberculosis Lung Polyomavirus (JC) CNS (PML) a a No shedding from these sites. b Formerly P. carinii. PML, progressive multifocal leukoencephalopathy. viral DNA in neurone (HSV, VZV) stem cell of epithelium (wart) bone marrow or spleen (CMV) reactivated virus random event? differentiation of cell? spread growth shedding lesion clinical A. primary reactivation event B. controllable by immune response Figure Two stages in reactivation of latent viruses. CMV, cytomegalovirus. 176 The second event (stage B) involves the spread and replication of the reactivated virus. HSV must travel down the sensory axon to the skin or mucosal surface, infect and spread in subepithelial tissues and then in the epithelium, finally forming a virus-rich vesicle ( > 1 million infectious units/ ml of vesicle fluid). All this takes at least 3 4 days. Stage B is less mysterious than stage A and can be controlled by the immune system. Therefore, cold sores may be associated with poor lymphocyte responses to HSV antigens, and zoster with declining cell-mediated responses (specifically to VZV antigens) in old people. Stage A probably occurs more frequently than stage B, because immune defences often arrest the process during stage B before final production of the lesion. Hence, as many as 10 20% of HSV reactivation episodes are thought to be non-lesional with burning, tingling and itching at the site, but no signs of a cold sore. Also, zoster may involve no more than the sensory prodrome associated with virus reactivation and replication in sensory neurones; skin lesions are prevented by host defences. Reactivation of EBV and CMV with appearance of the virus in saliva (EBV) or blood (CMV) is generally asymptomatic. In immunologically deficient individuals, however, reactivation may progress to cause clinical : either hepatitis and pneumonitis in the case of CMV or the rarer hairy tongue leukoplakia due to EBV (see Ch. 30 ).
5 KEY FACTS Many successful parasites have adopted strategies for evading immune responses. These enable them to stay in the body long enough to complete their business of and shedding to fresh hosts. Some parasites persist indefinitely in the body. Mechanisms of immune evasion include: concealing parasite antigens from the host (staying inside host cells, infecting privileged sites ) changing parasite antigens, either in the infected individual (trypanosomiasis) or during spread through the host population (influenza) direct action on immune cells (e.g. HIV on CD4 + T cells) or on immune signalling systems (e.g. production of fake cytokine molecules) local interference with immune defences (production of IgA proteases, Fc receptors). During s, the microbe may continue to multiply and be able to infect others (HIV, hepatitis B). Alternatively, during s, the microbe enters into a latent state and later in life reactivates with renewed multiplication and the ability to infect others (herpesviruses, M. tuberculosis ). 177
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