Pathogenesis of malaria and clinically similar conditions.
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Journal: 2004/September - Clinical Microbiology Reviews
ISSN: 0893-8512
Abstract:
There is now wide acceptance of the concept that the similarity between many acute infectious diseases, be they viral, bacterial, or parasitic in origin, is caused by the overproduction of inflammatory cytokines initiated when the organism interacts with the innate immune system. This is also true of certain noninfectious states, such as the tissue injury syndromes. This review discusses the historical origins of these ideas, which began with tumor necrosis factor (TNF) and spread from their origins in malaria research to other fields. As well the more established proinflammatory mediators, such as TNF, interleukin-1, and lymphotoxin, the roles of nitric oxide and carbon monoxide, which are chiefly inhibitory, are discussed. The established and potential roles of two more recently recognized contributors, overactivity of the enzyme poly(ADP-ribose) polymerase 1 (PARP-1) and the escape of high-mobility-group box 1 (HMGB1) protein from its normal location into the circulation, are also put in context. The pathogenesis of the disease caused by falciparum malaria is then considered in the light of what has been learned about the roles of these mediators in these other diseases, as well as in malaria itself.
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Clin Microbiol Rev 17(3): 509-539
PMID: 15258091

Pathogenesis of Malaria and Clinically Similar Conditions

School of Biochemistry and Molecular Biology, John Curtin School Of Medical Research Australian National University, Canberra, ACT 0200, Australia2
Corresponding author. Mailing address: School of Biochemistry and Molecular Biology, Australian National University, Canberra, ACT 0200, Australia. Phone: 61.2.6125.4363. Fax: 61.2.6125.0313. E-mail: ua.ude.una@kralc.nai.
Copyright © 2004, American Society for Microbiology

Abstract

There is now wide acceptance of the concept that the similarity between many acute infectious diseases, be they viral, bacterial, or parasitic in origin, is caused by the overproduction of inflammatory cytokines initiated when the organism interacts with the innate immune system. This is also true of certain noninfectious states, such as the tissue injury syndromes. This review discusses the historical origins of these ideas, which began with tumor necrosis factor (TNF) and spread from their origins in malaria research to other fields. As well the more established proinflammatory mediators, such as TNF, interleukin-1, and lymphotoxin, the roles of nitric oxide and carbon monoxide, which are chiefly inhibitory, are discussed. The established and potential roles of two more recently recognized contributors, overactivity of the enzyme poly(ADP-ribose) polymerase 1 (PARP-1) and the escape of high-mobility-group box 1 (HMGB1) protein from its normal location into the circulation, are also put in context. The pathogenesis of the disease caused by falciparum malaria is then considered in the light of what has been learned about the roles of these mediators in these other diseases, as well as in malaria itself.

Abstract

Four species of malarial parasite, members of a genus of protozoa within the suborder Haemosporidiidea, infect humans, and all are spread by female Anopheles mosquitoes. In practice, only one of these parasites, Plasmodium falciparum, causes fatal disease. It is the organism targeted in attempts to develop a malarial vaccine and is also the focus of research on antimalarial drug resistance. Therefore, references to malaria in this review are to falciparum malaria. Malaria stands out among the systemic infectious diseases of humans for many reasons, apart from the sheer scale of the problems it causes (344). Although it has been recognized as an entity for thousands of years, it was still thought to be noninfectious long after Pasteur had demonstrated that a number of other major diseases were caused by bacteria, and knowledge of its life cycle was not complete until 1951 (370). The relatively large P. falciparum is easy to locate within blood vessels in fixed tissue sections, and from the late 19th century (40), this characteristic allowed a plausible explanation of falciparum malarial disease, particularly its coma, in terms of poor oxygen delivery through partly obstructed blood vessels. This appeared to give malarial disease a unique pathogenesis, still with some currency today.

It is our view that focusing on malaria in isolation will never provide the insights required to understand the pathogenesis of this disease. How can the illnesses caused by a spirochete and a virus be so clinically identical (184), typhoid readily diagnosed as malaria (296), and malaria in returning travelers so commonly dismissed as influenza? Why do former military personnel with much personal experience of malaria invariably believe that the onset of brucellosis or Q fever is a relapse of malaria when they first seek out medical advice? An adequate explanation of malaria disease has to answer these questions. Understanding why these clinical confusions occur entails appreciating the sequence of events that led up to the cytokine revolution that has transformed this field over the last 15 years. To explain this adequately, we must outline the pathogenesis of these clinically overlapping systemic diseases caused by infectious agents other than malaria, as well as that of conditions such as burns, trauma, hemorrhagic shock, snakebite and heatstroke, which are not caused by specific microorganisms but which apparently have a similar molecular pathogenesis. An additional layer of complexity is provided by the fact that these molecules, often referred to as the proinflammatory cytokines, are also the basis of much cell-mediated immunity against infectious agents. We only touch on the recognition end of the spectrum of events that leads to the mediators of innate immunity and disease, which was comprehensively reviewed for bacterial infections recently in this journal (420). Instead, we concentrate on the current state of knowledge at the effector end of the process, where disease is actually generated. The pathogenesis of the more clinical aspects of falciparum malaria, such as hyperlactatemia, metabolic acidosis, hypoglycemia, respiratory distress, impaired consciousness, and anemia, has been reviewed recently (91).

Acknowledgments

Kirk Rockett, Dominic Kwiatkowski, Jean-Louis Virelizier, and Craig Boutlis are thanked for helpful discussions. Funded through the Wellcome Trust and NIH respectively, Malcolm Molyneux and Terrie Taylor provided a unique bank of human tissue, as well as their clinical expertise.

Funding from the Australian National Health and Medical Research Council, the Tropical Disease Research section of the World Health Organization, and at a crucial time from the Ben Brown Anti-Malaria Fund, is also gratefully acknowledged.

Acknowledgments

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