The Epidemiology of Plasmodium vivax

271 Pages·2013·6.438 MB·1-267\271

by  S.I. Hay, Ric Price and J. Kevin Baird (Eds.)

SERIES EDITORS
D. ROLLINSON S. I. HAY
Department of Zoology, Spatial Epidemiology and Ecology Group,
The Natural History Museum, London, UK Tinbergen Building, Department of
[email protected] Zoology, University of Oxford, South Parks
Road, Oxford, UK
[email protected]
EDITORIAL BOARD
M. G. BASÁÑEZ R. E. SINDEN
Reader in Parasite Epidemiology, Immunology and Infection Section,
Department of Infectious Disease Department of Biological Sciences,
Epidemiology Faculty of Medicine Sir Alexander Fleming Building, Imperial
(St Mary’s campus), Imperial College, College of Science, Technology and
London, London, UK Medicine, London, UK
S. BROOKER D. L. SMITH
Wellcome Trust Research Fellow and Johns Hopkins Malaria Research
Professor, London School of Hygiene and Institute & Department of Epidemiology,
Tropical Medicine, Faculty of Infectious Johns Hopkins Bloomberg School of Public
and Tropical, Diseases, London, UK Health, Baltimore, MD, USA
R. B. GASSER R. C. A. THOMPSON
Department of Veterinary Science, Head, WHO Collaborating Centre for
The University of Melbourne, Parkville, the Molecular Epidemiology of Parasitic
Victoria, Australia Infections, Principal Investigator,
Environmental Biotechnology CRC
N. HALL (EBCRC), School of Veterinary and
School of Biological Sciences, Biomedical Sciences, Murdoch University,
Biosciences Building, University of Murdoch, WA, Australia
Liverpool, Liverpool, UK
X. N. ZHOU
R. C. OLIVEIRA Professor, Director, National Institute of
Centro de Pesquisas Rene Rachou/ Parasitic Diseases, Chinese Center for
CPqRR - A FIOCRUZ em Minas Gerais, Disease Control and Prevention, Shanghai,
Rene Rachou Research Center/CPqRR - People’s Republic of China
The Oswaldo Cruz Foundation in the State
of Minas Gerais-Brazil, Brazil
VOLUME EIGHTY ONE
A
dvAnces in
PARASITOLOGY
Edited by
S. I. HAY
Spatial Epidemiology and Ecology Group
Tinbergen Building, Department of Zoology,
University of Oxford, South Parks Road,
Oxford, UK
RIC PRICE
Centre of Tropical Medicine,
University of Oxford,
Oxford, UK
J. KEVIN BAIRD
Eijkman-Oxford Clinical Research Unit
Jalan Diponegoro No. 69
Jakarta, Indonesia
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CONTRIBUTORS
Myriam Arevalo-Herrera
Caucaseco Research Center, Cali, Colombia
J. Kevin Baird
Eijkman-Oxford Clinical Research Unit, Jakarta, Indonesia; Centre for Tropical Medicine,
Nuffield Department of Clinical Medicine, University of Oxford, Oxford, UK
John W. Barnwell
Department of Medicine, Division of Infectious Diseases, Emory University School
of Medicine, Emory University, Atlanta, Georgia, USA; Centers for Disease Control
and Prevention, Malaria Branch, Division of Parasitic Diseases and Malaria, Atlanta,
Georgia, USA
Katherine E. Battle
Department of Zoology, University of Oxford, Oxford, UK
Jane M. Carlton
Center for Genomics and Systems Biology, Department of Biology, New York University,
New York, NY, USA
William E. Collins
Institutional Association: Malaria Branch, Division of Parasitic Diseases, Centers for
Disease Control and Prevention, Atlanta, Georgia
Aparup Das
Evolutionary Genomics and Bioinformatics Laboratory, Division of Genomics and
Bioinformatics, National Institute of Malaria Research (ICMR), Dwarka, New Delhi,
India
Ananias A. Escalante
Center for Evolutionary Medicine and Informatics, The Biodesign Institute, Arizona State
University, Tempe, AZ, USA
Marcelo U. Ferreira
Departamento de Parasitologia, Instituto de Ciências Biomédicas, Universidade de São
Paulo, São Paulo (SP), Brasil
Mary R. Galinski
Department of Medicine, Division of Infectious Diseases, Emory University School
of Medicine, Emory University, Atlanta, Georgia, USA; Emory Vaccine Center, Yerkes
National Primate Research Center, Atlanta, Georgia, USA
Simon I. Hay
Department of Zoology, University of Oxford, Oxford, UK
Rosalind E. Howes
Department of Zoology, University of Oxford, Oxford, UK
ix
x Contributors
Christopher L. King
Center of Global Health & Diseases (CGHD), Case Western Reserve University, V eterans
Affairs Medical Center, Cleveland, OH, USA
Odile Mercereau-Puijalon
Institut Pasteur, Centre National de la Recherche Scientifique Unité de Recherche
Associée, Unité d’Immunologie Moléculaire des Parasites, Paris, France
Esmeralda V.S. Meyer
Emory Vaccine Center, Yerkes National Primate Research Center, Atlanta, Georgia, USA
Ivo Mueller
Walter + Eliza Hall Institute, Infection & Immunity Division, Parkville, Victoria, Australia;
Barcelona Centre for International Health Research (CRESIB, Hospital Clínic-Universitat
de Barcelona), Barcelona, Spain
Jean-Louis Pérignon
Inserm, UMR-S 945, Paris, France; Faculté de Médecine Pitié-Salpêtrière, Université
Pierre et Marie Curie-Paris 6, CHU Pitié-Salpêtrière, Paris, France; Faculté de Médecine
Paris 5, Université René Descartes-Paris 5, CHU Necker-Enfants Malades, Paris, France
Ari W. Satyagraha
Eijkman Institute for Molecular Biology, Jakarta, Indonesia
Georges Snounou
Inserm, UMR-S 945, Paris, France; Faculté de Médecine Pitié-Salpêtrière, Université
Pierre et Marie Curie-Paris 6, CHU Pitié-Salpêtrière, Paris, France
Takafumi Tsuboi
Cell-Free Science and Technology Research Center and Venture Business Laboratory,
Ehime University, Matsuyama, Ehime, Japan
Peter A. Zimmerman
Center for Global Health & Diseases, Case Western Reserve University, Cleveland, Ohio,
USA
PREFACE
The epidemiology of Plasmodium vivax: history, hiatus and hubris forms is a
two volume special issue of Advances in Parasitology on the epidemiology of
P. vivax. The aim of the review collection is to present a contemporary sum-
mary of what is known about P. vivax, with the challenge set to the authors
to (1) retrieve what has been ‘lost’ from ‘history’, (2) summarize objectively
the current state of knowledge including the reasons for the ‘hiatus’ in inter-
est and; (3) identify research gaps/directions/priorities to gently temper the
prevailing ‘hubris’ with respect to control and elimination.
Part A (volume 80) was published in December 2012. It was composed
of six chapters and dealt principally with the most practical dimensions
of vivax malaria, describing the epidemiology, clinical consequences, treat-
ment, and control strategies shaped by the biology of the parasite. Part B
(volume 81) is published here and brings together a further six chapters that
investigate more fully aspects of the parasite life cycle, innate and inherited
aspects that confer host resistance to P. vivax infection, the epidemiological
importance of G6PD deficiency, what is known about the genome of
P. vivax and finally the lessons that can still be learned from the interpreta-
tion of the old neurosyphilis literature.
Chapter 1 by Mary R. Galinski and colleagues looks in detail at the para-
site’s life cycle, how it is adapted to its life history challenges and how this dif-
ferentiates it from P. falciparum. They also explore the research challenges that
remain in combining non-human primate models with new technologies
to potentially provide further insights and epidemiological understanding
of the biology of this parasite. Chapter 2, by Peter A. Zimmerman and col-
leagues, reviews fascinating new complexities to what is canonically taught
about red blood cell polymorphism (predominantly of the Duffy gene) and
susceptibility to P. vivax infection at the individual and population levels.
Chapter 3 led by Ivo Mueller reviews the natural acquisition of immunity
to P. vivax. Epidemiological observations are synthesised and used to support
the premise that a multi-stage P. vivax vaccine may be feasible. Chapter 4 by
Rosalind E. Howes reviews the geography of G6PD deficiency. The global
distribution of its prevalence and genetic variants are discussed along with
the implications that this has for the potential risk of haemolysis triggered
by primaquine therapy in different parts of the world. Chapter 5, written by
Jane M. Carlton and colleagues, considers the genomics, population genetics
xi
xii Preface
and evolutionary history of P. vivax. New insights from detailed genomic
investigations of P. vivax across India are synthesised, as well as, research
avenues opening as a result of next generation sequencing technologies,
discussed. In the final Chapter 6, Georges Snounou and Jean-Louis Péri-
gnon conclude these volumes by reviewing the epidemiological insights
gained from a thorough analysis of the malaria therapy for neurosyphilis
literature. They outline further some of the insights that might be gained in
relation to the current challenges of P. vivax epidemiology, immunology and
pathology by a deeper engagement with this literature.
It is perhaps worth noting that the enormous literature summarized in
these two volumes evidences a rich history that we are unwise to forget.
Moreover, that the authorship have perhaps helped turn the corner on the
research hiatus of P. vivax. Conversely, and perhaps predictably, it also reveals
there is much still to learn and therefore that we must approach with some
hubris the immediate challenges of P. vivax control and future challenges of
its elimination. Finally we take this opportunity to thank all the authors
for their considerable time and energy devoted to putting these chapters
together. We hope that these two volumes “lower the bar” for a new cohort
of malariologists inspired by future challenges in the epidemiology and
control of P. vivax.
Simon I. Hay, Ric N. Price and J. Kevin Baird
CHAPTER ONE
Plasmodium vivax: Modern
Strategies to Study a Persistent
Parasite’s Life Cycle
Mary R. Galinski*,†,1, Esmeralda V. S. Meyer†, John W. Barnwell*,‡
*Department of Medicine, Division of Infectious Diseases, Emory University School of Medicine,
Emory University, Atlanta, Georgia, USA
†Emory Vaccine Center, Yerkes National Primate Research Center, Atlanta, Georgia, USA
‡Centers for Disease Control and Prevention, Malaria Branch, Division of Parasitic Diseases and
Malaria, Atlanta, Georgia, USA
1Corresponding author: E-mail: [email protected]
Contents
1. I ntroduction 2
2. T heGeneralLifeCycleofPlasmodium vivaxandOtherPrimateMalaria
ParasiteSpecies 3
2.1. T heHypnozoite:AnAlternativeLifeStyleforLiver-stageDevelopment 6
2.2. T heReticulocyteasaHostCell:AnEnvironmentalSafetyProgramforP. vivax 8
2.3. F astandFurious:TheSexualLifeStrategiesofP. vivax 9
3. I n VitroandEx VivoModelsforExaminingP. vivaxBiology 11
4. N eotropicalNon-HumanPrimateModels(NewWorldMonkeys)forInvestigating
theVariedBiologyofvivaxMalaria 14
5. T heRelapsingMalariaParasitesofSouthernAsianMacaqueMonkeysas
ModelsforP. vivaxBiology 15
6. F romGenomicstoSystemsBiology:TheBiggerPicturePuzzles 17
7. C onclusions 20
Acknowledgements 20
References 20
Abstract
Plasmodium vivaxhasuniqueattributestosupportitssurvivalinvaryingecologies
andclimates.Theseincludehypnozoiteformsintheliver,aninvasionpreference
forreticulocytes,caveola–vesiclecomplexstructuresintheinfectederythrocyte
membraneandrapidlyformingandcirculatinggametocytes.Thesecharacter-
isticsmakethisspeciesverydifferentfromP. falciparum.Plasmodium cynomolgi
andotherrelatedsimianspecieshaveidenticalbiologyandcanserveasinfor-
mativemodelsofP. vivaxinfections.Plasmodium vivaxanditsmodelparasites
canbegrowninnon-humanprimates(NHP),andinshort-termex vivocultures.
Advances in Parasitology, Volume 81 © 2013 Elsevier Ltd.
ISSN 0065-308X, http://dx.doi.org/10.1016/B978-0-12-407826-0.00001-1 All rights reserved. 1
2 MaryR.Galinski et al.
ForP. vivax,intheabsenceofin vitroculturesystems,thesemodelsremainhighly
relevantsidebysidewithhumanclinicalstudies.Whilepost-genomictechnologies
allowforgreaterexplorationofP. vivax-infectedbloodsamplesfromhumans,these
comewithrestrictions.TwoadvantagesofNHPmodelsarethatinfectionscanbe
experimentallytailoredtoaddresshypotheses,includinggeneticmanipulation.
Also,systemsbiologyapproachescancapitaliseoncomputationalbiologycom-
binedwithsetexperimentalinfectionperiodsandprotocols,whichmayinclude
multiplesamplingtimes,differenttypesofsamples,andthebroaduseof“omics”
technologies.Opportunitiesforresearchonvivaxmalariaareincreasingwiththe
useofexistingandnewmethodologicalstrategiesincombinationwithmodern
technologies.
1. INTRODUCTION
Plasmodium vivax has been neglected as a disease of major global
i mportance. Recently, expanded efforts have been made to bring more
widespread attention to this disease and to overcome perceptions that
there are in surmountable barriers to advancing research and basic
knowledge on vivax malaria (Carlton et al., 2011; Galinski and Barn-
well, 2008; Lacerda et al., 2012; Mueller et al., 2009; Price et al., 2011).
In fact, research and methodological strategies are in place to move
forward using the most modern technologies available, and advances are
being made. Basic vivax malaria research is benefiting from the incor-
poration of ex vivo samples from humans, non-human p rimate (NHP)
experimentation and in vitro analyses. In addition, an increased focus on
the epidemiology of P. vivax, with an increased attention to interactions
with other species, and greater consideration of the ecological factors
that affect this parasite’s range is apparent (Gething et al., 2012). Various
clinical, epidemiological and biological attributes associated with vivax
malaria have also gained the attention of mathematical modellers and
computational biologists who wish to apply currently available knowl-
edge on the host and vector interactions with this parasite to understand
transmission and the influence of current control interventions and drug
treatments on those dynamics (Aguas et al., 2012; Chamchod and Beier,
2012; Gething et al., 2011; Mueller et al., 2009; Price et al., 2011; White,
2011). However, to improve modelling efforts and control strategies,
interventions or drug therapies will benefit from a better understand-
ing of the biological attributes that afford P. vivax and its sibling species
life strategies that enable it to persist when confronted with control
methods implemented by its human host.
Plasmodium vivax:ModernStrategiestoStudyaPersistentParasite’sLifeCycle 3
2. T HE GENERAL LIFE CYCLE OF PLASMODIUM VIVAX
AND OTHER PRIMATE MALARIA PARASITE SPECIES
In general terms, the life cycle of P. vivax is like that of all of the
other primate malaria species in that it requires an invertebrate and a verte-
brate host for survival and perpetuation; a female mosquito of a susceptible
Anopheles species and a primate, whether human or NHP (Fig. 1.1). When
the female mosquito bites, or more precisely, probes the dermis with her
proboscis looking for a vessel to obtain her blood meal, she releases salivary
fluid and along with it a few sporozoites from her salivary glands. In the
dermal tissues, the sporozoites are motile and capable of penetrating small
blood vessels, and beginning to stimulate a host immune response (Guilbride
et al., 2012; Sinnis and Zavala, 2008). In the circulating blood, they are swept
into the liver sinusoid vessels where they penetrate through the professional
phagocytes known as Küpffer cells into the Space of Disse to begin the exo-
erythrocytic or liver-stage cycle of growth (reviewed in Baer et al., 2007b;
Frevert et al., 2008; Meis et al., 1983; Pradel and Frevert, 2001). Once there,
the sporozoite then penetrates a hepatocyte, rounds up and differentiates
into a small trophozoite (∼4 µ in diameter) growing in size over the next
few days eventually differentiating into a multinucleated schizont in 5 days.
By 6 or 7 days, of primary growth and development, a fully mature schizont
40–60 µ in diameter has differentiated into thousands of individual invasive
single nucleated merozoites surrounded by a parasitophorous membrane
capsule. As reported for rodent malaria experimental model systems (not
yet investigated in primate malarias), the plasma membrane of an infected
hepatocyte breaks down, and blebs of the parasitophorous membrane full of
merozoites called merosomes break off and flow into the circulation of the
liver sinusoid vessels (Prudencio et al., 2006; Thiberge et al., 2007). These
merosomes are carried into the faster flowing general blood circulation and
break apart releasing the imprisoned merozoites (Baer et al., 2007a), which
then attach to and invade red blood cells (RBCs) to start the erythrocytic
cycle of infection, also known as the blood-stage cycle.
The newly invaded merozoite immediately differentiates into an eryth-
rocytic trophozoite and begins remodelling the anucleate RBC to provide
a suitable environment for it to grow larger over a period of 48 hours
feeding upon the haemoglobin of the parasitised RBC. Thirty-eight or 40
h into this cycle of growth, the nucleus divides in two to create a schizont
and over the next 8 or so hours continues to divide by schizogony to form