Climate Change and Mosquito-Borne Disease Source: …
Climate Change and Mosquito-Borne Disease Author(s): Paul Reiter Source: Environmental Health Perspectives, Vol. 109, Supplement 1: Reviews in Environmental Health, 2001 (Mar., 2001), pp. 141-161 Published by: The National Institute of Environmental Health Sciences (NIEHS) Stable URL: Accessed: 14/11/2008 05:41 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at . JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at . Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact support@.
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ClimateChange and Mosquito-BorneDisease
Paul Reiter
Dengue Branch, Division of Vector-Borne Infectious Diseases, National Center for Infectious Diseases, Centers for Disease Control and Prevention, U.S. Department of Health and Human Services, San Juan, Puerto Rico
Globalatmospheric temperatures are presently in a warming phase that began 250-300 years ago. Speculations on the potential impact of continued warming on human health often focus on mosquito-borne diseases. Elementary models suggest that higher global temperatures will enhance their transmission rates and extend their geographic ranges. However, the histories of three such diseases-malaria, yellow fever, and dengue-reveal that climate has rarely been the principal determinant of their prevalence or range; human activities and their impact on local ecology have generally been much more significant. It is therefore inappropriateto use climate-based models to predict future prevalence. Key words:.Aedes aegypti, anopheles, climate change, dengue, global warming, malaria, mosquito, public health, vector, yellow fever. - Environ Health Perspect
109(suppl 1):141-161 (2001). http.//ehpnet 1.niehs.docs/2001/suppl-1/141-161reiter/abstract.html
ClimateChange
Natural factors that cause climatic
variability include fluctuations of the sun's
The earth'sclimatehas alwaysbeen in a state radiant energy, alterations in the trans-
of change (1-3). For nearlythreecenturiesit parencyof the atmosphere(due to sand, vol-
has been in a warming phase. This was pre- canic dust, and other airborneparticles),and
ceded by a cold period, the Little Ice Age, cyclic changes of the earth's rotation on its
which was itself precededby a warmerphase axis and its orbit around the sun. In addi-
knownasthe MedievalWarmPeriod,or Little tion, the circulationsof the atmosphereand
ClimaticOptimum. Such changesareentirely the oceans, which are major components of
natural, but there is evidence that in recent the climate machine, are subject to internal
yearsa portionof the currentwarmingmaybe variationson time scalesrangingfrom weeks
attributableto human activities,particularly to millennia. It is the complex interactionof
the burningof fossilfuels(4-6). The potential all these variablesthat generatesthe continu-
impact of this global warming on human ally changingpatternsof climate.As a result,
healthis a majorsubjectof debate(7-10).
just as the yearly averages of climatic ele-
Many of the diseasesthat currentlyoccur ments-such as temperature, humidity,
in the tropics are mosquito borne (11). It is rainfall,wind, and airborneparticles-differ
commonly assumedthat their distributionis from one another,so too do the averagesfor
determinedby climateand thatwarmerglobal decades, centuries, millennia, and millions
temperaturews ill increasetheirincidenceand of years(Table 1).
geographic range (12-14). This review
Climate is a major parameter in all
exploresthe validity of both assumptionsby ecosystemsand has alwaysbeen a fundamen-
examiningthe historyof threemosquito-borne tal factor in human settlement, economy,
diseases-malaria,yellow fever,and dengue- and culture. Episodes of second-order cli-
in the context of past climates and of other mate change, such as the end of the Ice Age,
factorsthatcaninfluencetheirtransmission. the drying of the Sahara,the waning of the
Climate
MedievalWarm Period,and the onset of the LittleIce Age, have had an importantimpact
Climate (Greek KlktgLa, an inclination or on human history (1,2,15). However, aware-
slope-e.g., of the sun's rays;a latitude zone ness of such changehas remainedshadowyat
of the Earth) is commonly understood to best, probably because the inherent time
mean the averageweatherin a given regionor scales are beyond the span of individual
zone. In its olderform, climealso includedall human experience.
aspects of the environment, including the
During most of geologic history, temper-
zonaldistributionof plantsand animals.Both ate conditions extended to the polar circles,
definitions are unsatisfactory because they and the planet was relativelyice-free (3,16).
imply that, unlike the obvious year-to-year Indeed, in the perspective of the past 600
variations of daily weather, long-term climate million years, present global temperatures
is a constant. By contrast, modern climatol- are relatively cool. In the context of these
ogy recognizes that change is an inherent and long-term averages,the warming trend that
fundamental feature of climate. Therefore, began in the late 1970s (see below) is a
climatic values cannot be quoted without minor fluctuation, less than a first-order
specifying the time span to which they refer. variation.
Weathier
Weather, the short-term condition of climate,has a much more directand tangible impact on daily life. Since earliest times, weatherhas been fundamentalto the success of human activities,from agricultureto seafaring,from warfareto leisure.The universal belief in weather deities, the prominence of weather events in folklore, and the ubiquitous preoccupation with weather signs and portents are evidence that an awareness of weather, particularly a fear of inclement events, has been a major feature of the human psychethroughouthistory.
The significance of weather has not diminishedin modernsociety. Indeed,in the past few decades,weatherawareness,particularly in the global context, has reached unprecedentedlevels.Weatherforecastinghas becomean importantscience,fundamentalto the success of agriculture, transportation, trade, tourism, and virtually every other aspectof human enterprise.Weatherdataare collected from every corner of the globe and disseminatedin digestedform by government and private agencies as an aid to decision making in all walks of life. Continually updated forecastsand other information are availableto the publicvia the popularmedia. Disastrous weather events from around the world area majornews feature,with detailed descriptions and graphic illustration. With this awareness of weather has come a new realizationof the changeabilityof climate.
Recent Climate Change
Currently, world climate is in a warming phase that began in the early decades of the eighteenthcentury.Temperatures,at least in the Northern Hemisphere, are now broadly similarto what they were during the Middle Ages,in the centuriesbeforethe LittleIceAge (2). Awarenessof this warming has led to a new preoccupation: concern that human activitiesmay be affectingthe naturalclimatic
Addresscorrespondenceto P. Reiter,CDCDengue Branch1, 324CalleCanadaS, anJuan,PR00920-3860. Telephone: (787) 706 2399. Fax: (787) 706 2496. E-mailp: reiter@
I am gratefulto many people who gave helpful comments on the manuscript,especiallyD. Gubler, G. Clark,J. Rigau-Perez,S. Bernard,K.Ebi,and E. Reitera, ndto M.Wolcottforhelpwiththe figures.
Received 18 July 2000; accepted 27 September 2000.
EnvironmentalHealth Perspectives * VOLUM1E091 SUPPLEME1NMT arch2001
141
Reiter
Table 1. Timescaleofclimaticvariation.a
transmit. In the tropics, comparable
Order
Interva(lyears)
Descriptor
Examploef variation
adaptations are necessary for surviving in unfavorabledry periods, which can last for
1
30-100
Instrumenrtecord
2
100-1,000
Historical
3
1,000-10,000
Glacial
4
10,000-1 million
Minorgeologic
Coolingtrendfrom1940to late1970s MedievaWl armPeriodL, ittleIceAge Variatiown ithinanIceAge IceAge
several years. In both cases, such adaptations impose a seasonality on transmission. For example, before eradication, the trans-
5
1-100 million
Majorgeologic
IntervabletweenIceAges
mission season for Plasmodiumfalciparum
aGlobeavlentsuchastheElNinoSoutherOnscillatipohnenomenoocncuartafrequenwcyellbelowthatofthefirsotrdeorfvariation. in Italy was July-September (34). The
same 3 months constitute the malaria sea-
son in Mali, where the disease is still
regime,just as they arechangingmany other may alternate among birds, mammals, and aspectsof the environment.From the 1940s even reptiles. A complex salivary secretion to the late 1970s, when global temperatures facilitatesfeeding. It is the direct injection of
endemic (35). The physicalenvironmentis an important
modifierof localclimate(36). In denseforest,
werein decline,therewasconcernthat partic- this fluid into the capillaries that enables daily mean temperaturesat ground level can
ulateindustrialpollutantsmight be exertinga several life forms-viruses, protozoa, and be as much as 10?C lower than in adjacent
global cooling effect (17-19). Since then, as nematode worms-to exploit mosquitoes as open areas (37). Similarly, natural daytime
world climatesreturnedto a warmingmode, a meansof transferbetween vertebratehosts. temperaturesindoors can be severaldegrees
interesthas switchedto the greenhouseeffect, In nearly all cases, there is an obligatory higheror lower than outdoors,dependingon
a naturalphenomenonby which atmospheric phasewithin the insect. This includesa stage design, construction materials, and ventila-
gasestrapsolarradiationin the formof heat. in which they multiply prodigiously in the tion. Mosquitoesuse a varietyof strategiesto Although the principalgreenhousegas is salivary glands, from which they can be exploitthe timing and locationof such micro-
water vapor, about 2% by volume, public attentionfocusesmainlyon carbondioxide,a gas that is essentialas the ultimate source of
inoculated into a new host during a later climates to maximum advantage.For examblood meal. Although most such organisms ple, in Anophelesgambiae(38), a physiologic do not appearto affecteitherthe mosquitoes "clock"ensuresthatwhateverthe rateof meta-
carbonfor nearlyall life on the planet. From or their vertebratehosts, some arepathogens morphosis in the pupal stage, the adults
the mid-nineteenth centuryonward,massive of importanthuman and animaldiseases.
alwaysemergefrom the waterat sundown or
clearanceof forests for agriculture,followed by an exponential rise in the combustion of fossil fuels (coal, oil, gas), has produced a
Factors That Influence Transmission Climaticfactors. The ecology, development,
in the earlyhoursof the night. In the laboratory, if An. gambiaepupae are maintainedin constantlight, the durationof the pupalstage
measurable increase in atmospheric CO2 behavior,and survivalof mosquitoesand the is a direct function of temperature:It lasts
from around 0.029% in 1890 to 0.037% transmission dynamics of the diseases they about 2 days at 22?C but only 1 day at 32?C
today. Many climatologists agree that this transmit are strongly influenced by climatic (Figure1A). However,in a light regimeof 12
28% increase in atmospheric CO2 together factors.Temperature,rainfall,and humidity hr light and 12 hr dark(LD 12:12), the timwith an increase in other anthropogenic are especiallyimportant, but others, such as ing is modified(Figure1B) to minimizeemer-
greenhousegasesmay be contributingto the wind and the durationof daylight,can alsobe gence in daylight (39,40). Similar circadian
warming trend of recent decades (4-6,20). significant.The same factorsalso play a cru- rhythms ensure that other behaviorssuch as The extent of this contribution remains far cial role in the survivaland transmissionrate feeding,resting,and ovipositionarerestricted
from clear, but the mere possibility that of mosquito-bornepathogens. In particular, to optimum times, regardlessof ambienttemhumanactivitiesmay be involvedimpliesthat temperatureaffects their rate of multiplica- perature(41). Thus, An. gambiaecan survive the trend could be reversible,and has gener- tion in the insect.In turn, this affectsthe rate in the Sudan (mean monthly temperaturesof
ateda spiritedscientific(5,7,21-23) and public (24-26) discussion. Human health-and mosquito-borne disease in particular-is a
at which the salivary secretions become 42?C; actual outdoor temperatures can be infected,and thus the likelihoodof successful over55?C)by emergingaftersunset,hiding in transmission to another host. Of course, if the thatchof buildingsin the daytime,feeding
prominenttopic in this debate(12,27-32).
the development time of the pathogen after midnight, and ovipositing at dawn or
Mosquito-Borne Disease
exceeds the life span of the insect, transmis- dusk (42). sion cannot occur. It is the complex interplay Analogous survival strategies operate in
Mosquitoes As Vectors of Disease
of all these factorsthat determinesthe overall temperateclimates. Culexpipiens,a vector of effect of climate on the local prevalence of the St. Louis encephalitis virus (and the
Mosquitoes are found throughout the world mosquito-bornediseases(11,33).
recently imported West Nile virus), is com-
except in placesthat are permanentlyfrozen.
Seasonalityis a key componentof climate. mon in North America as far north as New
There are about 3,500 species, of which Summer temperatures in many temperate Brunswickand Nova Scotia, Canada.It over-
nearlythree-quarterasre nativeto the humid regionsare at least as high as in the warmest wintersin the adult stage,sequesteredat sites tropics and subtropics. The largest popula- seasonsof much of the tropics.The crucialdif- protectedfrom the cold. Here again,light (in
tions of individualspeciesoccur in the Arctic ferenceis thatthe tropicsdo not havecoldwin- this case, daylength) is the zeitgeberor cue tundra,where colossal numbersemerge in a ters.Tropicalcropssuchasriceandgroundnuts that initiates the survival strategy. Studies
single brood each summer from snowmelt can be cultivatedin temperateregionsif they (43) in Memphis, Tennessee, revealed a
pools thatoverliethe permafrost.
areplantedin springtime.Similarly,if tropical remarkably high winter survival rate (p =
In nearlyall mosquito species,the female mosquito-bornepathogensare introducedin 0.97) in an underground storm sewer.
obtains the protein she needs for the devel- the rightseason,theycanbe transmittedif suit- Survival was the same in a cold winter
opment of her eggs by feeding on vertebrate ablevectorsarepresent;in most casesthey are (1981-1982: 42 days of freezing tempera-
blood. Some species are highly selective, eliminatedwhenwintersetsin.
tures, mean daily minimum temperature
restricting themselves to one or at most a
Mosquitoes native to temperate regions [December 1-February28] -0.74?C; 9 days
few closely relatedhost species. Others have have had to evolve strategies to survive the with minimum of less than -10?C) as in a
a less clearly defined host preference and winter, as have the pathogens that they much warmer"ElNifo" winter(1982-1983;
142
VOLUME109 1SUPPLEMEN1T1March2001 * EnvironmentaHlealthPerspectives
Climatechange and mosquito-bornedisease
25 days of freezingtemperatures;mean daily minimum temperature [December 1February 28] +2.9?C; 1 day of less than -10?C, maximum temperatures as high as
27.2?C).
Memphis has a typical temperate continental climate. There are normallyabout 65 days per year with maximum temperatures above 32?C (temperatures above 38?C are not unusual) and about 60 days when the minimum fallsbelow 0?C (lows of-15?C are
not unusual)(44). Aedesaegypti,the principal urbanvectorof dengue and yellow fever,is a tropicalspeciesfor which temperaturesbelow 0?C arefatal.Nevertheless,at the time of the
studiesmentionedabove (and probablyfor at least200 yearsbefore),Ae. aegyptwi as present throughout the southern United States, and wascommon in Memphis.Presumablyit survived duringwinter in niches protectedfrom the cold. Despite the effectiveness of this strategy,in the past 15 years the species has disappearedfrommuch of the region,including Memphis, displaced by another nonnative species, Ae. albopictus (45). This example and the others given above emphasize that meteorologic variablesalone are of limited value as a guide to the development times, behavior,and geographicrangeof vector speciesandthe pathogensthey transmit.
Humanfactors.Human activitiesarealso crucialto transmission.Forestclearanceelim-
inatesspeciesthat breedin waterin treeholes (e.g., the forest Aedesspecies that transmit yellow fever) but provides favorable conditions for those that prefertemporaryground pools exposed to full sunlight (e.g., many of the Anophelesspecies that transmit malaria). Drainage of wetlands eliminates the marshy pools exploitedby many speciesbut can provide the open channels preferred by others (e.g., some important European vectors of malaria, and Culex tarsalis, a vector of St.
Louisencephalitis).Agriculturaflertilizerscan promote the growthof algaeand other larval nutrients, whereasherbicides may eliminate them altogether. Cisterns, pit latrines, sewage-polluted ditches, storm drains, and blockedgutterscan supportlargepopulations of Cx. quinquefasciatusa,n importantvector of BancroftianfilariasisW. ells areoften a significant source of malaria vectors. Water-
storage jars and drums, cemetery urns, discarded rubber tires, buckets, pots, and other man-made containers can be prolific sources of Ae. aegypti,an important peridomesticvectorof yellow feverand dengue and otherspeciesthatoriginallybredin treeholes.
Additional factors arise from behavior
and culturaltraits. Daily activity patternswork, rest, and recreation-the location of
homes in relation to mosquito breeding sites, the design of buildings, the materials used to build them, the use of screens and
A
50-
45-
40-
s 35-
a0(3D o
c 30-
C.-
0 , 15-
B I -
c a)
40I tLD12:12
OiLL
5o
34.
----32.0'
10-
.C0L
a)
__,-t~~27
10-
E
Ia/,)
______ L 4A. ___ L 24.50
_pI
A 22.0?
II.
l
l
22 24 26 28 30 32 34 36
0
24
48
Temperatu(r?eC)
Time(hr)
Figure1. Theinfluenceof lightregimeonthetimingof the emergenceof adultAn.gambiaefromthe pupalstageat differentemperatureisnthe laboratory(A. )Duratio(nmean+ SD)of the pupalstage inconstantlight(LL)(.B)Timing of emergenceinLLandina dailyregimeof 12hrlight:12hrdark(LD12:12)I. ntheLLregime(openhistogramsd,ownward)eclosionoccursas soon as metamorphosiiss complete.Inthe LD12:12regime(openhistogramsu, pward) emergenceis delayedto givea peaknearthe timeof light-offP. indicatesthe 6-hrperiodduringwhichthe pupae werecollectedinhourlybatches.Inthe laboratoryp,upationnormallpyeaks3-4 hrbeforethe endof the lightphase (41).Inthe field,pupationandpupal/aduletclosionare bothdelayeduntilsunset(187)orthereafter.Physiologic "gates"of thistypemaintainregularrhythmosf physiologyandbehaviorregardlessof the effectsof temperature. FigurereprintefdromReiterandJones(39),withpermissionof BlackwelSl cienceLtd.
bed nets, and many other factorscan be significant. Finally,chemotherapy,vaccination, and mosquito control have played major roles in reducingtransmissionin many parts of the world.
Predictingthe Impactof Climate Change
Transmission models. Much of the recent speculationon the possibleeffectsof climate change on mosquito-borne disease has focused on rudimentary concepts of their transmissiondynamics(30,46-48). An example is vectorialcapacity,a convenientway of expressingtransmissionrisk:
C mapn -loge P
where m is the mosquito density per human, a is the averagenumber of bites per day for each mosquito,p is the probabilityof a mosquito survivingthroughany one day, and n is the extrinsic incubation period-the time takenfor the pathogento developin the mosquito until the insect becomes infective.The only factordirectlyaffectedby a climatevariableis n, which is inverselyrelatedto temperature. Because p is less than unity, pn will increaseat higher temperatures,although p itselfmay decreaseas a resultof other factors. However, the denominatoris an exponential function,so p, survivalrate,is dominant.
Caged mosquitoes can live for 3-4 months, but their median age in the field is commonly about 4-6 days.Clearly,in nature few die of senescence; most are killed by predators, disease, and other hazards long before they reach old age (49). Feeding and the search for oviposition sites are probably the most hazardous activities. Species that become inactive (e.g., in winter or in the dry season)are known to survivefor as long as 9 months.
Vectorialcapacityand similarelementary models were developedto explorethe fundamental featuresof the transmissionof mos-
quito-borne disease (50-53), mainly in the context of mosquito control operations. Exceptfor n, the calculationof C dependson quantitativevaluesthat can be obtainedonly in the field. However, it is hard to estimate
these values realisticallybecause their measurementdependsheavilyon a complex range of assumptions(54-57). Moreover, C is limited to entomologicparametersand the duration of extrinsic incubation; it does not
incorporate the parasite rate in humans or mosquitoes, nor any of the many ecologic and behavioralfactorsoutlined in the previous section. Thus, although helpful in our understandingof transmissiondynamicsand as a practicaltool in specific situations,such models have a limited value for assessingthe impact of long-term climate change on diseasetransmission(58,59).
EnvironmentHalealthPerspectives* VOLUM1E091 SUPPLEME1N1MT arch2001
143
Reiter
An alternativeapproachis to look at the the genus Homo and have affected humans times until about A.D. 400 (2). Landscape
past. The historyof mosquito-bornediseases since theirearliestdays.
studiessuggesta gradualrise in sea level over
at differentlatitudesand in differentclimatic
The clinicalcourseof malaria(33) generally this period. Around 300 B.C., beech trees
erascan help us assessthe significanceof cli- involvesdistinctivebouts of feveralternating (genusFagus)grew in Rome, the Tiber River
mate variables in the context of the many with periods of freedom from illness. Each froze in winter, and snow lay for many days.
otherfactorsthat affecttransmission.
episodebeginswith a shortperiod (15 min-1 However, by the first century A.D. the
Historyof climates.Climatologyis a rela- hr) of violent shivering,with the patienthav- Romans considered the beech a mountain
tivelyyoung science.Apartfrom a handfulof ing cyanoticlips and fingers,a rapidbut weak tree, and winters were definitely less severe.
sites, systematic records of climate variables pulse, and a feeling of intense cold (rigor). Over these centuries, the cultivation of the
areavailableonly for the pastcentury,mainly This cold stage is followed by 2-6 hr of dis- vine and olive moved gradually northward
from land-based stations in the Northern tressing heat, accompanied by flushed skin, alongthe Italianpeninsula.The Romanswere
Hemisphere. Global data, obtained by intenseheadaches,nausea,and a full, bound- even able to introduce wine growing to
weather satellites, are availableonly for the ing pulse.The hot stageis followedby profuse Germanyand Britain, and import data sug-
past few decades. Thus the time span of sweating and a rapid drop in temperature, gest that Britainbecameself-sufficientin wine
direct studies of climate is within the first often to levelsbelownormal.
productionby aroundA.D.300. The warming
order of climatic variation, less than the
A prominent featureof the febrile bouts trend is clearlyindicatedby tree-ringstudies
periodforvalidlong-termchange(Table 1). is their periodicity:They tend to recurevery in California,so it mayhavebeen a worldwide
Fortunately,a largeamount of alternative third day with Plasmodium.vivax, P. falci- or at leasta hemisphericphenomenon(2).
data is available. Documentary information parum, and P. ovale and every fourth day
The firstliterarymention of an autumnal
fromannals,chronicles,auditedaccounts,agri- with P. malariae. From earliest times this feveris in Homer'sIliad(800 or 900 B.C.),as
culturalrecords,tax ledgers,and a wealth of periodicity gave rise to the descriptors tert- Achillessetsout to fightHector (61):
other archivalmaterialprovidesa rich source of indirect information, particularlyon the timing and occurrence of extreme weather eventssuchas drought,flood, or unusualcold. Descriptions of wind direction, wind speed,
ian and quartan fevers. Another common term was aestivo-autumnalor harvestfever becausein temperateregionsepidemic transmission tended to occur in late summer and
autumn (33).
Andold KingPriamwasfirstto seehim coming, surgingoverthe plain,blazinglike the star thatrearsatharvestf,lamingup in its brilliancefaroutshiningthecountlessstarsin thenightsky, thatstartheycallOrion'sDog-brightest of all
cloudformations,and otherweatherindicators are availablefrom privatediaries,ships' logs, Malaria in Temperate Climates
buta fatalsignemblazonedon theheavens, it bringssuchkillingfeverdownon wretchedmen.
accounts of military campaigns, and similar Prehistory. About 60 species of Anopheles
sources.Substantiallines of evidenceare also can transmit human malaria. Those that
We cannot be certain that this was
availablefromarchaeologicg,eologic,fossil,and exist in Europe probably began colonizing malaria,but the referenceto killing feversat
othersources.They includethe studyof glacial the regionas the ice capsretreatedat the end harvesttime is one that recursmany times in
moraines, lake and ocean sediments, pollen of the Pleistocene epoch. Human popula- other descriptionsof malaria.Latertexts con-
strata,depositsof insects,treerings,coralstruc- tions, also moving northward, almost cer- firmthat the diseasehad become a significant
ture, radiometric analysis of ice cores, and tainly brought malariaparasitesalong with featurein Greeklife. Indeed,thereis evidence
manyotherindicatorsA. ll this evidencemakes them. The prevalence of the disease in the that a majorwave of malariabegan with the
it possibleto realisticallyreconstructpast cli- Neolithic period and the Bronze Age is floweringof Greekcivilizationand transmis-
matesoverthe courseof time (2,16).
uncertain, but it is unlikely to have been sion rates continued to increase throughout
History of mosquito-borne disease. The veryhigh becausehuman groupswere gener- the period of the Roman Empire (2,62). scientific study of mosquito-bornediseaseis ally small and widely scattered.Nevertheless, Hippocrates(460-377 B.C.)gave exquisitely
alsolimitedto the past 100 years.Fortunately, early Neolithic skeletal remains from detaileddescriptionsof the courseand relative
the symptoms of three important diseases- Anatolia and Macedonia exhibit pathologic severity of tertian versus quartan infections
malaria,yellow fever,and dengue-are fairly changesthat have been attributedto chronic (63). He alsonoted theirassociationwith wet-
distinctive.Thus, as with climatology,we can anemia caused by P. falciparum infection. lands and even observed that splenomegaly turn to a variety of sources for evidence of The widespread presence of thalassemia (enlargedspleen,often a symptomof chronic
theiroccurrencein past climates.The bulk of (Mediterraneananemia), a genetic condition malariainfection)was particularlyprevalentin
this review is devoted to such evidence. that gives some protection against malaria, peoplelivingin marshyareas.
Particularemphasisis placedon the temperate may also indicate a long history of contact
PraxagorasH, eraclides,and other medical
latitudes because of the wealth of historical with the pathogen.
writersgave similardescriptions,from which
materialsthat is availableand becausemodels
Ancient Greeceand Rome.The introduc- it appearsthat much of Greece had become
suggest that the impact of global warming tion of agriculture,around 7000 B.C., led to highlymalarious(62).
maybe greatestat theselatitudes.
increasedpopulationsof relativelysettledpeo-
There is a wealth of evidencethat malaria
Malaria
ple and increasinglyfavorableconditions for was common in imperialRome (34). Horace, malaria transmission (34). The extensive Lucretius,Martial, and Tacitus were among
The Disease
deforestationthat beganat this time may also many Latin authorswho mentioned the dishave contributed to prevalence by creating ease. The Pontine Marshes,close to the city,
Malaria(Italianmalaaria,bad air)is a proto- additionalhabitatfor anophelinemosquitoes. were notorious as a source of infection.
zoan (genus Plasmodium)infection transmit- Similar ecologic changes in modern times Marcus Terentius Varro (116-127 B.C.)
ted by mosquitoes of the genus Anopheles. have causedmajorincreasesin the prevalence describedthese locapalustria(feverareas)and
The four species of Plasmodiumthat infect of the disease.
attributed the disease to animalia quaedam
humans appearto have evolved from a com-
Contemporaryaccountstogetherwith fos- minuta quae nonpossuntoculi consequi(ani-
mon ancestor during the early Tertiary sil and other evidence suggest that a gradual mals too small to be seen). He advised that
period,some 60 millionyearsago (60). Thus, warming and drying occurred in the houses should be built in high, well-
some or all of them probablyco-evolvedwith Mediterranean region throughout classical ventilatedplacesso that the bestiolaethat bred
144
VOLUM1E09 1SUPPLEME1NIMT arch2001 * EnvironmentHalealthPerspectives
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