Atmospheric Movement of Microorganisms in Clouds of Desert Dust and Implications for Human ...

19 Pages·2007·0.46 MB·English

CLINICALMICROBIOLOGYREVIEWS,July2007,p.459–477 Vol.20,No.3
0893-8512/07/$08.00(cid:1)0 doi:10.1128/CMR.00039-06
Atmospheric Movement of Microorganisms in Clouds of Desert Dust
and Implications for Human Health
Dale W. Griffin*
U.S.GeologicalSurvey,St.Petersburg,Florida33701
INTRODUCTION.......................................................................................................................................................459
OCCURRENCE...........................................................................................................................................................461
Bacteria....................................................................................................................................................................461
Fungi.........................................................................................................................................................................465
Viruses......................................................................................................................................................................465 D
PATHOGENS..............................................................................................................................................................466 o
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Bacteria....................................................................................................................................................................466
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Fungi.........................................................................................................................................................................466 lo
Viruses......................................................................................................................................................................467 a
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UnknownAgents.....................................................................................................................................................469 e
DETECTION...............................................................................................................................................................470 d

Collection.................................................................................................................................................................470 fr
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Identification............................................................................................................................................................471
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CONCLUSIONSANDPERSPECTIVES.................................................................................................................472

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ACKNOWLEDGMENT..............................................................................................................................................472
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REFERENCES............................................................................................................................................................472 p
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INTRODUCTION to-year dust flux have been previously reported (73, 74, 156,
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166,189,191,192,212,224,235). .a
The larger deserts on the planet, which include the Sahara s
andSahelregionsofNorthAfricaandtheGobi,TaklaMakan, DuststormactivityinthedesertsofAsiaisseasonal,withthe m
majorityofatmospherictransportoccurringduringthespring .
and Badain Jaran deserts of Asia, are the primary sources of o
(February to May) (258). Although Asian dust generation is r
mobilized desert top soils that move great distances through g
seasonal, significant quantities are generated and can be dis- /
theatmosphereeachyear(Fig.1).Thecurrentestimateforthe o
annual quantity of desert dust that makes regional or global perseduniversallyintheNorthernHemisphere.AlargeAsian n
dusteventin1990movedacrossthePacific,theNorthAmer- J
airbornemigrationsis0.5to5.0billiontons(184).Whileitis a
believed that the Sahara and Sahel regions of North Africa icancontinent,andtheAtlanticOceanandwaslateridentified n
intheFrenchAlpsviaisotopicanalysisofdepositedparticulate u
havebeenandarethedominantsourcesofdustintheatmo- a
matter (84). A large dust event impacting the west coast of r
sphere (50 to 75% of the current estimate), there has been y
increased Asian dust activity over the last 20 years that has NorthAmericain1998reducedsolarradiationlevelsby30to 1
40%andleftachemicalfingerprintofdepositeddustextend- 2
beenattributedtoclimatechangeanddesertification(73,166, ,
inginlandtothestateofMinnesota(100). 2
191, 265). Between 1975 and 1987, the desertification rate in 0
Chinawas(cid:2)2,100km2year(cid:3)1(266).Otherregionsofknown Asian dust storms can take from 7 to 9 days to cross the 1
PacificOcean.DuststormsmovingoffthewestcoastofAfrica 9
dust storm activity include the arid regions of the continental
can take from 3 to 5 days to reach the Caribbean and Amer- b
United States (the Great Basin), Central America, South y
America (Salar de Uyuni), Central Australia, South Africa icas.AsFig.1illustrates,continuoustransmissionofftheNorth g
Africandesertscanresultinprolongedexposureofindividuals u
(EtoshaandMkgadikgadibasins),andtheMiddleEast(244). e
livingatconsiderabledistances(theCaribbeanandAmericas) s
In general, high-energy wind conditions in arid regions can t
fromthesourceofparticulates.Usingahandheldlaserparticle
resultinthemobilizationofsignificantquantitiesofsoilsinto
counter,Irecordedabackgroundparticulateloadof2.6(cid:4)106
the atmosphere, and large dust storm events are capable of
continent-wide,transoceanic,andglobaldispersion(68,193). airborne particles m(cid:3)3 at a location south of Tampa Bay,
Dust emanates from North Africa year-round and at times Florida, on 15 July 2005. During an African dust event that
throughout the year impacts air quality in Africa, the Middle occurred from 25 to 28 July 2005, the particle count in the
East,Europe,Asia,theCaribbean,andtheAmericas(Fig.2). same region south of Tampa Bay on 25 July was 26.1 (cid:4) 106
DustsourceareasintheSaharaandSahel,primarylatitudinal particlesm(cid:3)3.Ninety-ninepercentoftheparticleswerewithin
transport routes, and the influence of climate and climate asizerangeof(cid:5)0.3(cid:6)mto(cid:7)1.0 (cid:6)m,thesub-2.5-(cid:6)mfraction
systems(NorthAtlanticOscillationandElNin˜o,etc.)onyear- thatcanpenetratedeepintothelungenvironment(Fig.1Cis
an image of that dust event period). These data demonstrate
the ability of dust storms to impact air quality at significant
distancesfromtheirsources(TampaBayis(cid:5)6,500kmwestof
*Present address: U.S. Geological Survey, 2010 Levy Ave., Talla-
hassee, FL 32310. Phone: [phone], ext. 3062. Fax: (850) 942- the coast of North Africa). A higher risk to human health
9521.E-mail:dgriffi[email protected]. wouldobviouslybeassociatedwithpopulationsclosertodust
459
460 GRIFFIN CLIN.MICROBIOL.REV.
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FIG. 1. AfricanandAsianduststorms.Starsidentifydustcloudsourceregions,andarrowsidentifydustcloudsandthegeneraldirectionof :/
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movement.(A)NASAimage,viathemoderate-resolutionimagingspectroradiometer(MODIS)aboardtheTerrasatellite,ofaduststormblowing c
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overtheSeaofJapanon1April2002.(ImagecourtesyofJacquesDescloitres,MODISLandRapidResponseTeam,NASA/GoddardSpaceFlight
r
Center.)(B)NASAimage,viaMODIS,ofaduststormblowingoutofAfricaovertheMediterraneanSeainthedirectionofTurkey.Theblack .
a
spotinthetongueofdustistheTroo¨dosmountainrangeofCyprus,whichprotrudesthroughthetopofthedustcloud.Theimagewastakenon s
25 February 2006. (Courtesy of Jeff Schmaltz, MODIS Land Rapid Response Team, NASA/Goddard Space Flight Center.) (C) NASA Sea- m
ViewingWideField-of-ViewSensor(SeaWiFS)imageofalargedustcloudblowingacrosstheAtlantic.Theimagewastakenon19July2005and .
o
iscourtesyoftheSeaWiFSProject,NASA/GoddardSpaceFlightCenter,andORBIMAGE.ThisdustcloudimpactedtheairqualityinFlorida. r
AirborneparticlemeasurementstakenbytheauthorwithahandheldlaserparticlecountersouthofTampaBay,FL,wentfrom2.6(cid:4)106m(cid:3)3 g/
on15July2005(normalclearatmosphere)to26.1(cid:4)106m(cid:3)3on25July2005(dustconditions).Over90%oftheparticlesrangedfrom(cid:5)0.3to o
0.5(cid:6)minsize. n

J
a
n
source regions, as this excerpt regarding the American Dust deposition rate of ultrafine particles ((cid:7)100 nm) in the lungs ua
Bowlperiodillustrates: has been shown to increase as particle size decreases and to ry

increasewithexerciseversusresting(46).Healthstudiescon- 1
Itisstatedbysomeauthoritiesthatmanbreathes, 2
ducted in urban and suburban environments have demon- ,
onanaverage,approximately25poundsofairdaily.
strated mortality risk with exposure to particulate matter and 2
Nelson’s “Loose Leaf Living Medicine” says that a 0
have attributed this risk to anthropogenic particulates gener- 1
normal individual inhales 30.5 cubic inches of air at 9
ated through automotive and industrial combustion versus
eachbreathandbreathes17timesperminute.Then b
thoseofcrustalorigin(130,210).Severalstudiesconductedto y
withanaverageof0.0368gofdustpercubicfootof
investigatetheroleofduststormsthatconsistofconcentrated g
air over a period of ten hours (the average duration u
crustalparticulateshaveshownanassociatedallergic,asthma, e
of the dust storms) the straining apparatus of the
and silicosis/pulmonary fibrosis risk (36, 127, 173, 180, 202, s
respiratory system is confronted with a very large t
259). Areas impacted by desert dust storms, such as commu-
task.Fromabovefiguresitcanbecomputedthatan
nitiesintheMiddleEastandtheCaribbean,areknowntohave
individual breathes 6.6240 g of dust during an aver-
someofthehighestincidencesofasthmaontheplanet(8,16,
ageduststorm(18).
96). On the Caribbean island of Barbados, the incidence of
Everyhumanbreathtakenisladenwithparticulatematter, asthmaincreased17-foldbetween1973and1996,aperiodthat
andhumanevolutionproducedthemostobviousandfamiliar coincidedwithincreasedfluxofAfricandusttotheareaofthe
front line of defense, nose hair. Less obvious are the mucus island (97, 188). Gyan et al. recently demonstrated a link be-
glandsthatlineourairways.Theseglandsfunctiontotrapand tween African dust and pediatric respiratory stress on the
aidintheexpulsionofparticulatesviasecretion,ciliatedtrans- southern Caribbean island of Trinidad (85). Allergens com-
port,andingestionorcough.Ofparticularconcernareparti- monlyassociatedwithduststormsincludefungalspores,plant
cles of (cid:7)10 (cid:6)m in size that can penetrate into the lungs and andgrasspollens,anthropogenicemissions,andorganicdetri-
thoseof(cid:7)2.5(cid:6)mthatmaypenetrateintodeeplungtissueand tus(62,103,125).
thesubepithelialenvironment.Theseverysmallparticlescause Desert dust cloud toxicity may be influenced by anthropo-
adverse health effects via oxidative stress (47, 52, 263). The genic material as a result of particulate/pollutant aerosoliza-
VOL.20,2007 DESERT DUST MICROBIOLOGY AND HUMAN HEALTH 461
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FIG. 2. Primarysourcesofdesertdustandtheiratmosphericpathways.(1)DuringsummerintheNorthernHemisphere(approximatelyJune

throughOctober),AfricandesertdustistransportedacrosstheAtlantictothenorthernCaribbeanandNorthAmerica.(2)Duringwinterinthe fr
o
NorthernHemisphere(approximatelyNovemberthroughMay),AfricandesertdustistransportedacrosstheAtlantictothesouthernCaribbean m
andSouthAmerica.(3)TheAsiandustseasontypicallylastsfromlateFebruarytolateApril.(4)LargeAsiandusteventscantravelsignificant

distancesintheNorthernHemisphere.YellowlinesshowAsiandesertdustatmosphericroutes,orangelinesshowAfricandustroutes,brownlines h
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show routes of other desert dust sources, and broken black lines depict wind patterns. (Base map image courtesy of NASA’s Geospatial tp
InteroperabilityOffice,GSFC[http://viewer.digitalearth.gov/].) :
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tionduringcloudformationorcloudcaptureduringdownwind shift through time due to climatic and geologic change (148, a
s
transport (adsorption of pesticides, herbicides, and industrial 163). m
emissions,etc.).Inherenttoxicityisduetodifferencesinnative .o
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soilelementalcomposition(metalsandnaturallyoccurringor g
OCCURRENCE /
syntheticradioisotopes,etc.),atmosphericchemicalalteration,
o
sizefractionation,andextremeparticulateload(5,44,88,131, Reflectingonthewholeofthis,Iconcludethatthe n

174,176,263).Toxicmetalssuchasarsenicandmercuryhave germs float through the atmosphere in groups or J
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been shown to occur in airborne desert dust in downwind clouds, and that now and then a cloud specifically n
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environments at concentrations higher than regional crustal different from the prevalent ones is wafted through a
concentrations(93).Inadditiontothepresenceofthesetoxic theair.ThetouchingofanutritivefluidbyaBacteria ry
metals, dust can indirectly impact human health by spurring cloudwouldnaturallyhaveadifferenteffectfromthe 1
2
toxic algal blooms in coastal environments (i.e., red tides, in touching of it by the sterile air between two clouds. ,

which marine organisms utilize dust components such as iron But, as in the case of a mottled sky, the various 2
0
asanutrientinnutrient-depletedwaters)(93,138,243).Dust portions of the landscape are successively visited by 1
9
cloudsmaycontainhighconcentrationsoforganicscomposed shade,so,inthelongrun,arethevarioustubesofour
b
ofplantdetritusandmicroorganisms(80,108)andmaypickup tray touched by the Bacterial clouds, the final fertil- y
additional biological loads (fungal spores, bacteria, viruses, izationorinfectionofthemallbeingtheconsequence g
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and pollen, etc.) as the clouds move through and sandblast (236). e
downwind terrestrial environments and/or over aquatic envi- s
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ronmentsthroughtheadhesionofmicrobe-ladenfineaquatic
Bacteria
spraystodustparticles.Allofthesepotentialdustcloudcon-
stituents may negatively influence human health in regional Deserttopsoilsareladenwithviableanddiverseprokaryote
and downwind environments, with the greatest risk factors communities(29,32,53,124,177).Globally,agramoftopsoil
beingfrequencyofexposure,concentrationofandcomposition contains (cid:2)107 (forest) to 109 (arid and other soil types) pro-
of particulates, and immunological status. Dust-borne micro- karyotes (247). These populations are believed to consist of
organisms in particular can directly impact human health via (cid:2)10,000 bacterial types with (cid:2)0.1% of the total population
pathogenesis,exposureofsensitiveindividualstocellularcom- composing(cid:2)99.9%ofthediversity(67,233,234).Studiesthat
ponents (pollen and fungal allergens and lipopolysaccharide haveexaminedthenumberofculturableprokaryotesindesert
[LPS],etc.),andthedevelopmentofsensitivities(i.e.,asthma) soils have reported concentrations ranging from 0 to (cid:2)107
throughprolongedexposure.Dust-bornedispersionofmicro- gram(cid:3)1(126,144,169).
organismsmayalsoplayasignificantroleinthebiogeographical Dominantphylafoundinsoils,asdeterminedbytheirprev-
distribution of both pathogenic and nonpathogenic species, as alenceinsequencelibraries,includetheProteobacteria,Acido-
long-range atmospheric transport routes and concentrations bacteria, and Actinobacteria (110). Although this community
462 GRIFFIN CLIN.MICROBIOL.REV.
TABLE 1. Generaofbacteriaandfungifoundinduststormsampleswhereidentifiedtoatleastthegenuslevela
Methodofidentification
Bacterialgenus/genera Fungalgenera Location(reference) Dustsourceregion
(bacterial/fungal)
Arthrobacter,Bacillus, Alternaria,Cryptococcus,Mortierella, Fattyacidmethylestersand Kuwait(141) MiddleEast
Cryptococcus,Flavimonas, Penicillium,Phoma,Rhodotorula, 16SrRNAgene
Kurthia,Neisseria,Paenibacillus, andStemphylium sequencing/26SrRNA
Pseudomonas,Ralstonia,and genesequencing
Staphylococcus
Bacillus,Pseudomonas,and Alternaria,Aspergillus,Botrytis, Microscope/microscope SaudiArabia(126) SaudiArabia
Staphylococcus Cladosporium,Mortierella,Mucor,
Penicillium,PythiumUlocladium,
andVerticillium
Arthrobacter,Corynebacterium, Alternaria,Cladosporium, 16SrRNAgenesequencing/ Turkey(82) Sahara
Microbacterium,Nocardioides, Microsporum,andPenicillium microscopeand18S
Planococcus,Saccharothrix,and rRNAgenesequencing D
Streptomyces o
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Arthrobacter,Agrococcus,Bacillus, Acremonium,Alternaria, 16SrRNAgenesequencing/ Turkey(82) MiddleEast n
Curtobacterium,Duganella, Cladosporium,Fusarium, microscopeand18S lo
Kocuria,Massilia,and Microsporum,Penicillium,and rRNAgenesequencing a
Microbacterium Trichophyton d
e
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ND Alternaria,Aspergillus,Cladosporium, NA/microscope Israel(207) Sahara
Coleophoma,Fusarium,Libertella, fr
o
Lophiostoma,Penicillium,Phoma,
m
andZygosporium

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Acinetobacter,Agrococcus, Cladosporium,Alternaria,and 16SrRNAgenesequencing/ Mali,Africa(117) Sahara/Sahel tt
Arthrobacter,Aureobacterium, Aspergillus 18SrRNAgene p
:
Bacillus,Corynebacterium, sequencing //
Deinococcus,Dietzia,Gordonia, c
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Kocuria,Microbacterium,
Micrococcus,Paenibacillus, r.
Paracoccus,Planococcus, a
s
Rhodococcus,Saccharococcus, m
Staphylococcus,Streptomyces,
.
andZoogloea o
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g
Actinomyces,Bacillus, Alternaria,Cladosporium, 16SrRNAgenesequencing/ Tropicalmid-Atlantic Sahara/Sahel /

Brevibacterium,Cellulomonas, Dendryphion,Lojkania, 18SrRNAgene ridge(83) o
Frigoribacterium,Gordonia, Lithothelium,Massaria,Myriangium, sequencing n

Kocuria,Lechevalieria, Neotestudina,Penicillium,Phoma, J
Leifsonia,Lentzea, Setosphaeria,Stachybotrys, a
n
Novosphingobium, Trichophyton,andUlocladium u
Pseudomonas,and a
Staphylococcus r
y

Actinosynnema,Afipia,Agrococcus, Acremonium,Aspergillus, 16SrRNAgenesequencing/ U.S.VirginIslands Sahara/Sahel 1
2
Ancylobacter,Arthrobacter, Aureobasidium,Bipolaris, 18SrRNAgene (78,79) ,
Bacillus,Bosea,Curtobacterium, Chromelosporium,Chrysosporium, sequencing 2
Frankiaceae,Fulvimaria, Cladosporium,Coccodinium, 0
Hymenobacter,Kocuria, Cochliobolus,Geotrichum, 1
Kineococcus,Mesorhizobium, Gibberella,Microsporum, 9

Nocardioides,Paracoccus, Monocillium,Nigrospora, b
Propionibacterium, Oidiodendron,Paecilomyces, y

Pseudomonas,Rhizobium, Penicillium,Pleospora,Rhizomucor, g
Saccharothrix,Sphingomonas, Scytalidium,andTrichophyton u
e
Sinorhizobium,Streptomyces,
s
andTaxeobacter t
Bacillus ND Microscope/NA Sweden(20) NorthoftheBlackSea
Bacillus Myceliasterilia(unidentifiedimperfect Microscope/microscope Barbados(190) Sahara/Sahel
fungiwithnoknownsporestage,
48%ofisolates),Alternaria,
Arthrinium,Aspergillus,
Cladosporium,Curvularia,
Neurospora,Penicillium,and
Periconium
ND Fusarium,Aspergillus,Penicillium,and NA/microscope Korea(261) Gobi/TaklaMakan
Basipetospora
ND Penicillium,Aspergillus,Nigrospora, NA/microscope Korea(256) Gobi/TaklaMakan
Arthrinium,Curvularia,Stemphylium
Cercospora,andPithomyces
Continuedonfacingpage
VOL.20,2007 DESERT DUST MICROBIOLOGY AND HUMAN HEALTH 463
TABLE 1—Continued
Methodofidentification
Bacterialgenus/genera Fungalgenera Location(reference) Dustsourceregion
(bacterial/fungal)
ND Alternaria,Arthrinium,Aspergillus, NA/microscope Taiwan(92) Gobi/TaklaMakan
Botrytis,Cercospora,Cladosporium,
Curvularia,Drechslera,Fusarium,
Ganoderma,Nigrospora,Papulara,
Penicillium,Periconia,Pithomyces,
Stemphylium,andUlocladium
aAllstudieslistedwereculturebased.ND,nodata;NA,notapplicable.
composition is determined by a number of factors, including lates collected from the atmosphere over the mid-Atlantic
pH, temperature, elemental composition, and nutrient and ridge((cid:2)15°N,45°W)duringperiodsofelevatedAfricandesert D
moisturecontent,membersofotherphylaalsooccurlessfre- dust concentrations consisted of 13 genera, with those domi- o
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quently(67,110).Pigmentsproducedbydesertsoiltaxasuch nantbeingBacillus(32%),Gordonia(12%),andStaphylococ- n
as Nostoc sp. and Scytonema sp. are believed to provide UV cus (8%) (83). When African dust was visibly present in the lo
a
shielding compared to less-pigmented community members northernCaribbeanair,asubsetofisolatesfromvarioussam-
d
(21). Novel or rare actinomycetes (Citricoccus alkalitolerans, pleswasidentifiedby16SrRNAgenesequencesasconsisting e
d
Jiangella gansuensis, and species of Nocardiopsis and Saccha- of 25 genera (78, 79). The most dominant genera detected in
f
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rothrix)havebeenisolatedfromanumberofdesertsoilsam- these samples were Microbacterium (14.4%), Sphingomonas o
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plescollectedinthedesertsofbothAfricaandAsia(216,267). (7.2%), Bacillus (6.5%), and Streptomyces (4.0%). Eleven of

Similartothepotentialhazardsoflifeinthesoil,atmospheric the isolates (closest GenBank neighbor) had previously been h
t
sourcesofstresstoairbornemicroorganismsincludeUVdam- identified in marine environments, demonstrating that aero- tp
:
age, desiccation (drying by wind), temperature (both low and solizedmarinespraymayadheretodustparticlesastheclouds /
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high temperatures depending on the tolerance range of an move over marine environments (78, 79). The few other dust m
organism),andatmosphericchemistry(humiditylevelsdepen- storm-relatedstudiesdevotedtotheprevalenceofbacteriain r
.
dent on tolerance and oxygen radicals, etc.) (54, 76, 158). atmosphericsampleswerebasedonthepresenceofspores(in a
s
Dust-borne transport of microorganisms, particularly over aerobic culture; i.e., species of Bacillus were identified) or m
aquatic environments, should be enhanced due to tolerable othercellularmorphologies(19,126,190)orononlyreported .o
r
humiditylevelsandattenuationofUVbytheparticleloadof CFU(39). g
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the various dust clouds (78). NASA research has shown that Concentrationsofbacteriaobservedduringduststormsare
o
the particle load of large dust clouds can attenuate UV by notedinTable2.BetweenAprilandNovember1934,30flights n

morethan50%(91). were conducted at altitudes of 0 to 7,772 m in the vicinity of J
a
Table1liststhegeneraidentifiedinduststormmicrobiology Boston,MA,tocollectairsamplesformicrobialanalysis(187). n
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studies as described below. While it would be interesting to Flight4recoveredsamplesataltitudesof457to7,772mata a
compareandcontrastthediversityofisolatesidentifiedineach time when visibility was hampered by dust transported within ry

study, it should be noted that some relied on microscopy for airmassesfromoverthetropicalAtlantic(areaoftheSargasso 1
2
identification while others employed molecular methods. It Sea). These samples resulted in the growth of 16 to 266 bac- ,

shouldalsobeemphasizedthatallwereculture-basedstudies teria (overall average of the five samples, 144) and 11 to 43 2
0
andfewutilizedlikeassays(i.e.,collectionandculturemedia, fungi (overall average of five samples, 23) m(cid:3)3 of air (187). 1
9
etc.),whichrestrictsthecomparisonofdata. TheseCFUcountswerebyfarthehighestcombined(bacterial
b
DesertdustresearchinKuwait,whichfocusedon“military andfungal)countsforalloftheflights(fortheother29flights, y

personnel health protection,” identified 147 bacterial CFU, therewere137samplesyielding0to138bacterialCFU,aver- g
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which included representatives from 10 genera, by gas chro- age14,and0to267fungalCFU,average11).Flight4wasthe e
matographicanalysisoffattyacidmethylestersand16SrRNA onlyflightofthe30tobeaffectedbyTransatlanticdust(187). s
t
genesequencinginsettleddust(141).Sevengenerawereiso- InKansas,in1935,numbersofbacteriaonnutrientagarsettle
lated from the atmosphere over Erdemli, Turkey, during Sa- platesexposedtoduststormsrangedfrom2,880to42,735m(cid:3)2
harandusteventsinMarch2002,withthemostprevalentbeing min(cid:3)1(23).Imagesofaclear-daypetridishandaduststorm
species of Streptomyces (82). During a dust event of Middle petridish(bothplatesexposedtotheatmospherefor1.5min.)
East origin that impacted the same location in October 2002, showed fewer than 10 colonies isolated on the clear day and
speciesfromeightgenerawererecovered,withthemostprev- overgrowthontheduststormplate(23).Atmosphericsamples
alent belonging to the genus Kocuria (82). In Bamako, Mali, collected by plane from three altitudes (365, 1,280, and 2,500
Africa,Kelloggetal.identifiedasmallsubsetoftheobserved m)overJunction,TX,demonstratedthatthehighestconcen-
(n (cid:8) 94 [by 16S rRNA gene sequencing]) airborne bacterial trations of bacterial and fungal isolates occurred when dust
isolates collected during four dust events and one nondust generated by frontal activity was present (66). Graph-based
event.Theseisolateswerecomposedof20genera,andBacillus datashowed(cid:5)1,544combinedCFUm(cid:3)3atthe365-maltitude
sp. represented 38% of the isolates, followed by Kocuria sp. versus(cid:7)450combinedCFUm(cid:3)3ateachofthethreealtitudes
(12.8%), Planococcus sp.(8.5%), Saccharococcus sp. (7.4%), duringnormal/no-dustconditions.ThelowestCFUcollections
and Micrococcus sp. (6.4%) (117). Twenty-five bacterial iso- ((cid:7)100 at each altitude) followed frontal precipitation events
464 GRIFFIN CLIN.MICROBIOL.REV.
TABLE 2. Concentrationsofculturablebacteriaandfungiandfungalsporesinduststorms
Samplesite Concnb(bacterialCFUm(cid:3)3)(avg) Concnc(fungalCFUm(cid:3)3)(avg)
Duststormsource Samplingmethoda
(reference) Background Dust Background Dust
Boston,MA(187) Airmassfrom Oil-saturatedlens 0–138(14) 16–266(144) 0–267(11) 11–43(23)
overthe paperfroma
SargassoSea plane;altitudes,
0–7,620m
Kansas(23) Kansas Forbackground,1.5 Photographofoneplate 2,880–42,735 ND ND
min;fordust withlessthan10
storms,5-to15-s colonies
exposuresof
nutrientagar
settleplates
Junction,TX(66) Texas Exposureofnutrient (cid:7)450(avg)combined (cid:5)1,544(avg)combined Seebacterialconcn Seebacterialconcn
agarplatesfroma bacterialandfungal bacterialandfungal
plane;altitudes, CFU;NS CFU;NS
D
365–2,500m
SaudiArabia SaudiArabia Dustplatetrap ND 1,892(cid:9)325(100(cid:4) ND 869(cid:9)75(40(cid:4) o
w
(126) followedbya increaseover increaseover
n
dilutionmethod background) background)
(also6-hnutrient lo
a
agarsettleplate
d
counts) e
Mali(117) Sahara/Sahel (cid:7)1h,low-flow 200–1,100(537) 720–15,700(6,194) 0–130(62) 80–370(195) d
rate;MF
f
Israel(207) Sahara 25min,28.3liters 79–108(93) 694–995(844) 31–115(73) 205–226(215) r
min(cid:3)1;Andersen om
sampler
Turkey(82) Sahara/region (cid:7)1h,low-flow 0–41*(3) 0–59†(6) 0–291*(25) 0–703†(66) h
rate;MF tt
Tropicalmid- Sahara/Sahel (cid:7)1–12h,low-flow NA 0–24(1)‡ NA 0–27(3)‡ p
:
Atlantic(15°N, rate;MF //
45°W)(83) c
U.S.Virgin Sahara/Sahel (cid:7)1h,low-flow 0–100(12) 90–350(203) 0–60(15) 30–60(48) m
Islands(78) rate;MF r.
U.S.Virgin Sahara/Sahel (cid:7)1h,low-flow 1–100(13) 0–353(80) 0–57(13) 0–90(31) a
Islands(79) rate;MF s
Barbados(190) Sahara/Sahel (cid:2)24h,low-flow 0–((cid:2)10)(NS) 0–((cid:2)20)(NS) 0–((cid:2)4)(NS) 0–((cid:2)16)(NS) m
rate;MF .o
Korea(39) Gobi/TaklaMahan Andersensampler 105–1,930(386) 225–8,212(1,642) 100–8,510(1,702) 336–6,992(1,398) r
g
Taiwan(92) Gobi/TaklaMahan Sporetrap ND ND 4,839 6,078
/
Taiwan(256) Gobi/TaklaMahan Sporetrap ND ND 28,683 29,038 o
n
aLow-flowrate,(cid:7)20litersmin(cid:3)1;MF,membranefiltration.
bValuesfortheKansasstudyarebacterialcellspersquaremeterpermin.NA,notapplicableduetosomelevelofdustalwaysbeingpresent;ND,nodata;NS,not Ja
specified(graph-baseddata);*,dustconcentrationbelow12(cid:6)gm(cid:3)3;†,dustconcentrationatorabove12(cid:6)gm(cid:3)3;‡,dustconcentrationabove6(cid:6)gm(cid:3)3at10mabove n
sealevel. u
cValuesfortheTaiwanstudiesaremeannumbersofsporespercubicmeter.NA,notapplicableduetosomelevelofdustalwaysbeingpresent;ND,nodata;NS, a
notspecified(graph-baseddata);*,dustconcentrationbelow12(cid:6)gm(cid:3)3;†,dustconcentrationatorabove12(cid:6)gm(cid:3)3;‡,dustconcentrationabove6(cid:6)gm(cid:3)3at10m ry
abovesealevel. 1
2
,

2
0
(66). In Saudi Arabia, an increase of 100% over background trations(average,143.1CFUm(cid:3)3;n,8)occurringduringlate 1
9
levels was observed during dust storms with a settle plate July and early August (79). Dust-borne microbial concentra-
b
technique. Kellogg et al. (117) reported background levels of tionsintheearlysummer(May,June,andearlyJuly)werenot y
200 to 1,100 bacterial CFU m(cid:3)3 in the atmosphere over Ba- distinguishableabovenormalbackgroundlevelsinthisCarib- g
u
mako,Mali,Africa,anddustconditionlevelsrangingfrom720 bean research site (79). To determine if bacteria and fungi e
to15,700bacterialCFUm(cid:3)3.DuringtwoSaharandustevents being transported to the Caribbean in the early summer s
t
impacting Israel’s atmosphere (January and April 2004), air- monthsofMayandJunecouldbedetectedinairsamplesata
borne bacteria averaged 844 CFU m(cid:3)3, versus a 2-day back- site closer to the continent of Africa, a study was conducted
ground average of 93 CFU m(cid:3)3, and ratios of total CFU over the mid-Atlantic ridge at 15°N over a 6-week period (22
(bacteria and fungi) for dust days versus non-dust days were May to 30 June 2003). Results showed that bacterial CFU
similar to those reported by Griffin et al. in the Caribbean rangedfrom0.1CFUto23.7CFUm(cid:3)3whenculturablebac-
(207).AtErdemli,Turkey,dusteventbacterialconcentrations teria were recovered from the air samples (12 of 85 samples)
rangedfrom0to59CFUm(cid:3)3(average,6),versusbackground (83). The U.S. Navy’s Naval Aerosol Analysis and Prediction
concentrations of 0 to 41 CFU m(cid:3)3 (average, 3) (82). In the System, an atmospheric model that can determine airborne
northern Caribbean ((cid:2)18°N), normal background concentra- aerosol concentrations at various altitudes on a global scale
tions of bacteria in air samples collected over the islands and (94,114,196,209),demonstratedthatmostofthemicroorgan-
open water averaged 13.6 CFU m(cid:3)3 (28 samples) (79). The ismsrecoveredinthemid-Atlanticstudywererecovereddur-
same study noted an increase in airborne bacterial CFU (av- ingperiodsofelevatedaerosol(dust)concentrations(83).On
erage,80.1CFUm(cid:3)3[15samples])whenAfricandesertdust theislandofBarbados,at(cid:2)13.1°NinthesouthernCaribbean,
wasvisiblypresentintheatmosphere,withthehigherconcen- Africandesertdust-bornebacterialCFU(morphologicaliden-
VOL.20,2007 DESERT DUST MICROBIOLOGY AND HUMAN HEALTH 465
tifications were via spore staining, and almost all were identi- (78, 79, 82, 117). Concentrations of fungal CFU and spores
fiedasBacillussp.)rangedfrom0.0toapproximately20.0CFU observed during dust storms at various geographical loca-
m(cid:3)3,withthehighestconcentrationsoccurringprimarilydur- tionsarenotedinTable2.Inallcases,withtheexceptionof
ingthesummer(190).DuringAsiandusteventsimpactingair thedatareportedbyChoietal.(39)(Table2),thepresence
quality in Taejon, Korea, the bacterial CFU concentration of desert dust in the atmosphere resulted in an increase in
increasedonaverage4.3timesoverthatobservedundernor- the concentration of culturable fungi or fungal spores rela-
malatmosphericconditions(39). tive to background or clear atmospheric conditions.
Fungi Viruses
The total number of fungal species has been estimated at Viral abundance in soil has been shown to occur at a
1.5 (cid:4) 106, with approximately 7.4 (cid:4) 104 to 1.2 (cid:4) 105 having concentration of (cid:2)108 per gram (198, 252). Certain desert
beenidentified(89).Thenumberoffungitypicallyfoundina soil characteristics (high temperatures, elemental composi-
gramoftopsoilisapproximately106(225).Oneofthegenetic tion[theabilityofvirusestoadsorbtosoilparticulates],soil D
advantagesthatfungihaveovermanyothermicroorganismsis chemistry[pH],andmoisturecontent)areknowntoimpact o
w
that they are capable of producing spores. Spores enhance viral survival and thus community composition and concen- n
survival during transport and periods of prolonged environ- tration (260). Poliovirus and bacteriophage MS2 survival in lo
a
mentalstress.Fungalsporesareegg-likevesiclescoveredwith seeded desert soil samples was limited in the summer
d
a thin layer of hydrophobic proteins that provide protection months when temperatures of (cid:2)33.0°C and a decrease in e
d
from physical stresses such as UV exposure and desiccation soilmoisturecontent(from40%to(cid:7)5%)wererecorded(in
f
r
(56). Viable fungi recovered from extreme altitudes in the comparisontowintersurvival)(222).LowpH,lowmoisture, o
m
atmosphere have demonstrated the ability to survive harsh andhighconcentrationsofclay,cations,andtotaldissolved

conditions (77, 142, 143, 153, 200, 242). Mycological studies solidshavebeenshowntoenhancevirussurvivalbyincreas- h
t
conductedindesertenvironmentshavedemonstratedthatdi- ingadsorptionofvirusestoothersoilconstituents(99,215, tp
:
verse communities exist in desert topsoils worldwide (1, 2, 9, 260). As in soil, milder temperatures and moderate to high /
/
c
165,218).Anearlyreviewofoutdoorairborneconcentrations humidity (50 to 80%, depending on the virus type) favor m
offungalsporesreportedthatthehighestconcentrationstyp- viral survival in aerosols, with atmospheric transport over r
.
icallyoccurintemperateandtropicalregions(106sporesm(cid:3)3 open bodies of water (higher humidity versus that of over- a
s
ofair)andthelowestindesertenvironments(400sporesm(cid:3)3 land environments) favoring long-range dispersion and in- m
ofair)(129). fection (70, 104, 217). Bacteriophages that integrate their .o
r
In a survey of airborne fungi in the eastern and western genome into the host genome (prophage) may be more apt g
/
desertsofEgypt,44generaand102species(Aspergilluswas to survive long-range atmospheric transport than are viru-
o
thedominantgenus)wererecovered,withtheareasofhigh- lentphages(phagesthatdirectlyreplicateandlysehostcells n

est fungal concentrations and diversity corresponding to following infection and therefore do not benefit from the J
a
increases in vegetative cover and anthropogenic activity shielding potential of a host cell). The scientific community n
u
(107). The most prevalent fungal genera in airborne dust hasyettoaddressthistopicofresearch.Sinceprophagesare a
samples collected from the atmosphere of Taif, Saudi Ara- persistent in environmental bacterial populations and are ry

bia,were(31generaand70species)Aspergillus, Drechslera, important vectors of bacterial virulence factors (and other 1
2
Fusarium,Mucor,Penicillium,Phoma,andStachybotrys,and genomicmaterial),theseorganismsmayplayanunforeseen ,

it was noted that genus prevalence was dependent on the role in the global dispersion of prokaryotic genomic infor- 2
0
nutrient medium used (3). A similar study conducted in mation through long-range atmospheric dispersion (30, 1
9
Egypt identified 27 genera (64 species), and again, preva- 146). Viral transmission in aerosols (influenza viruses and
b
lencewasdeterminedbythenutrientmediumemployed(4). rhinoviruses, etc.) has been reviewed, and most of the doc- y

While most studies have shown that desert environments umented cases have been limited to short-range laboratory g
u
harbordiversemycologicalcommunities,fungisuchasCoc- tests (animal and human hosts) or indoor studies in hospi- e
cidioidesimmitisandCoccidioidesposadasiiareknowntobe tals (206). Data referencing long-range transmission of in- s
t
restrictedgeographically(theAmericasinthiscase)(90).In fectious viruses have been obtained only with aerosol mod-
contrasttomicrobialstudiesofsoilorairenvironments,far els (no field detection of the aerosolized virus) (206).
fewer studies have been devoted to dust-borne transport of Several papers have hypothesized transoceanic movement
microorganisms. Table 1 lists those fungal genera found in of viruses through the atmosphere based on favorable at-
duststormstudieswheredust-associatedisolateswereiden- mospheric conditions (i.e., wind patterns, mild tempera-
tifiedtoatleastthegenuslevel.Severalstudies,whileiden- tures) and incidence of disease (81, 87). One research
tifying bacterial and or fungal isolates, did not distinguish project that used a direct-count assay (use of a nucleic acid
thoserecoveredduringclearversusdustconditionsandthus staintocountmicroorganismsviaepifluorescencemicroscopy)to
are not included in Table 1 (66, 187). As can be seen from tabulatethenumberofvirus-likeparticlesinU.S.VirginIsland
Table 1, the dust-associated fungal community is diverse, atmospheric samples reported a background concentration of
and the true extent of diversity is probably much greater 1.8(cid:4)104m(cid:3)3andanAfricandusteventconcentrationof2.13(cid:4)
given that some of the more recent studies, which used 105m(cid:3)3(78).Insummary,littleresearchhasbeenconductedto
molecularmethodsforidentification,identifiedonlyasmall address the naturally occurring populations of desert soil viral
fraction of the cultured isolates due to budget constraints communities,thosevirusesintroducedbyhumansandotheran-
466 GRIFFIN CLIN.MICROBIOL.REV.
imals,oroccurrenceandsurvivalissuesassociatedwithairborne tions of African dust were present in the atmosphere (83).
desertsoils. Furthermore,atmosphericdust-bornebacteriaisolatedinthis
mid-Atlantic study that are recognized as pathogens included
Brevibacteriumcasei(opportunistic,sepsis)andStaphylococcus
PATHOGENS epidermidis (opportunistic, endocarditis, urinary tract infec-
tions) (22, 254). In the atmosphere over the U.S. Virgin Is-
Bacteria
lands, the opportunistic pathogen Pseudomonas aeruginosa,
Culture-based dust-borne microbiological studies have es- whichcancausefatalinfectionsinburnpatients,wasisolated
tablishedthatadiversebacterialcommunitycanmovethrough when African dust was present (79). Additionally, identified
the atmosphere in clouds of desert dust, but no study has microorganisms found in a Nigerian noma lesion study were
demonstrated the movement of a prokaryote pathogen and also isolated (GenBank closest neighbor similarities: Kocuria
linked it to the occurrence of disease. The closest known as- sp.,97%;Microbacteriumarborescens,98%;Sphingomonassp.,
sociationsofduststormsandhumandiseaseofmicrobialori- 96%) (79). At Erdemli, Turkey, Kocuria rosea, Corynebacte-
ginaretheoutbreaksofmeningitis(primarilyduetoNeisseria riumaquaticum(opportunistic,urinarytractinfections,sepsis), D
meningitidis infection) that occur within the “meningitis belt” andMassiliatimonae(whichhasbeenisolatedfromtheblood o
w
ofNorthAfrica(223).Theseoutbreaksoccurfrequentlyinthe ofanimmunocompromisedpatient)wereisolatedduringdust n
SahelregionofNorthAfricabetween(andwithin)themonths events (82, 133, 162, 226). Other desert dust studies included lo
a
ofFebruaryandMayandaffectasmanyas200,000individuals isolates of Bacillus, although no specific species-level patho-
d
annually (160, 223). The conditions during this period are genicidentificationsweremade(20,190). e
d
characterizedasdrywithfrequentduststorms.Outbreaksusu- ThebacterialendotoxinLPScanalsodirectlyimpacthuman
f
r
ally cease with the onset of the wet season (160, 161). Dust health via inhalation (205). LPS is a cell wall component of o
m
storms are believed to promote infection via dust particles gram-negativebacteriaandiscommonlyfoundinorganicdusts

causingabrasionsofthenasopharyngealmucosauponinhala- (240). Human and animal inhalation trials have shown in- h
t
tion,allowingNeisseriameningitidiscellsresidinginthemucosa creases in neutrophils and lymphocytes with a reduction in tp
:
accesstounderlyingtissueandblood,thusinitiatinginfection alveolarmacrophagephagocytosis(205).Short-termexposure /
/
c
(161). An additional and complementary hypothesis argues can result in fever and reduced airflow. Long-term exposure m
that cells of Neisseria meningitidis associated with the inhaled canresultinthedevelopmentoflungdiseasessuchasasthma, r
.
dustparticulatesareanalternaterouteofinfection(80). bronchitis, and irreversible airflow obstruction (240). Since a
s
Five viable isolates of Neisseria meningitidis recently identi- gram-negative bacteria are dominant in marine waters, aero- m
fiedinsettled-dustsamplesfromKuwaitdemonstratethatdust solizedmarinebacteriathatadheretotraversingdustparticles .o
r
canserveasacarrierforthepathogen(141).Otherpathogens may enhance dust cloud toxicity and affect human health in g
/
were also identified in this project (141), including Staphylo- coastalenvironmentsthataretypicallyimpactedbysignificant
o
coccus aureus (wide range of infections), Bacillus circulans, quantitiesofdesertdust.Africandustreachescoastalcommu- n

(opportunistic),Bacilluslicheniformis(opportunistic,peritoni- nities in Europe, the Middle East, the Caribbean, and the J
a
tis),Pantoeaagglomerans(opportunistic,peritonitis),Ralstonia Americas.AsiandustreachesKorea,Taiwan,Okinawa,Japan, n
u
paucula, (opportunistic, septicemia, peritonitis, abscess, and regionalislands,theArtic,andNorthAmerica.Approximately a
tenosynovitis), and Cryptococcus albidus (opportunistic, dis- halfofthebacteriafoundinAfricanduststudiesconductedin ry

seminated) (13, 122, 136, 140, 159, 179). Given the current theCaribbeanweregram-negativebacteria.Giventhevolume 1
2
stateofaffairsintheMiddleEast,manyoftheseopportunistic of annual African dust exposure, LPS may contribute to the ,

dust-borne pathogens may play a significant role in human high incidence of asthma in the region (79, 96). Sea spray 2
0
health with regard to combat-related injuries, treatment, and generationinnear-shoreenvironmentsmayalsoproduceele- 1
9
recovery. vatedhumiditylevelsinnear-surfaceatmosphericlayers,which
b
Bacterial species that are known human pathogens have canbothconcentrateand“rainout”dust-bornepathogensand y

beencollectedduringdusteventsinBamako,Mali(117).The toxins,thusincreasingexposureandrisk. g
u
species include Acinetobacter calcoaceticus (nosocomial respi- It is obvious from the few dust-borne microbiology studies e
ratory tract infections), Corynebacterium aquaticum (urinary that have identified pathogenic bacteria that there is some s
t
tract infections), Gordonia terrae (nervous system, skin), a degree of human health risk associated with exposure to air-
Kocuria sp. found in advanced noma lesions in Nigerian chil- borne desert dust. While most of the pathogens identified to
dren,andKocuriarosea(bacteremia)(10,28,55,117,147,181, dateareopportunisticinnature,thesearebutasmallnumber
226).Additionally,Acinetobactercalcoaceticushasbeenlinked ofculture-basedstudies,andasinmostoutbreaksofdiseaseit
to mad cow disease, and another isolate, Staphylococcus xylo- is often the young, old, and immunocompromised who are
sus, was previously identified as the causative agent of septi- within the higher levels of risk. These few studies provide a
cemia in a loggerhead turtle in the Canary Islands (117, 229, glimpse of risk evidence and highlight the need for non-cul-
232).Ofthe95bacteriaidentifiedinthisstudy,Kelloggetal. ture-basedassaystoadvancethisfieldofstudy.
reportedthatapproximately10%werepotentialanimalpatho-
gens, 5% were potential plant pathogens, and 25% were op-
Fungi
portunistichumanpathogens(117).IntheAfricandustcorri-
doroverthemid-Atlanticridge,twoofthehumanpathogens In 1941 several air fields were established in the
identified in the Mali dust study (83, 117), Kocuria rosea and southern San Joaquin Valley. Coccidioidal infection
Gordoniaterrae,werealsorecoveredwhenelevatedconcentra- wasrecognizedtobeahazard,butitwaspreferredto
VOL.20,2007 DESERT DUST MICROBIOLOGY AND HUMAN HEALTH 467
thehazardsofmountainsandfoginalternativeloca- Acremonium,Alternaria,Arthrinium,Aspergillus,Cladosporium,
tions. During the first year clouds of dust billowed Curvularia, Emericella, Fusarium, Nigrospora, Paecilomyces,
overthefields,andaquarterofthesusceptibleper- Pithomyces,Phoma,Penicillium,Torula,Trichophyton,andUlo-
sonnelbecameinfected.C.E.Smith,appointedcon- cladium). Outside of human disease, an outbreak of aspergil-
sultant to the Secretary of War, proposed rigid dust losiswasdocumentedinacaptivelocustpopulation((cid:2)40%of
controlmeasures.Roadswerepaved,airstripswere thepopulation)inBikaner,India,followingaduststorm(239).
hard-surfaced,andswimmingpoolsweresubstituted Sahara/Sahel dust storms have also been identified as long-
for dusty athletic fields. Lawns were planted by the range transport mechanisms for the pathogen responsible for
acre,andmilitarypersonnelwereordered,atriskof the Caribbean region-wide outbreak of Aspergillus infections
courtmartial,toavoidunprotectedareasasmuchas (A.sydowii)inseafans(213,245).Thelong-rangeatmospheric
possible(64). dispersaloffungalcroppathogenshasbeenwelldocumented.
BrownandHovmøllerpresentareviewofthosedata(24).
The most well-known human pathogen associated with
desertduststormsisthefungusCoccidioidesimmitis(64).This
D
fungushasbeenfoundonlyintheAmericas.Annualoutbreaks Viruses o
followingduststorms(theprimarymeansofexposure)ordust w
Transportofinfectioushumanvirusesinduststormshasnot n
clouds generated from natural disasters or anthropogenic ac- been investigated. Hammond et al. hypothesized that long- lo
tivity (e.g., earthquakes and construction, etc.) are well docu- a
range transport of human influenza virus from Asia to the
d
mented(90,113,178,208).AnoutbreakataNavalAirStation Americascouldoccurinthewintermonthsgiventheprevailing e
in California following a large dust storm event resulted in a d
wind patterns over the Pacific and the low dose of virus re-
f
coccidioidomycosis incidence rate of 36 per 100,000 for per- r
quired for infection (87). With the annual peak of the Asian o
sonnel classified as white and 254 per 100,000 for those clas- m
dust season occurring in March and April, the attachment of
sifiedasnonwhite,indicatingdifferencesinracialsusceptibility infectious viruses to dust particles moving across the Pacific h
(250). In Arizona, an increase in annual cases from 33 per may serve to enhance long-range host-to-host transport, as ttp
100,000 in 1998 to 43 per 100,000 in 2001 was attributed to :
virus survival studies (water and air based) have shown a re- /
/
climatechange(increasedwindspeedanddrought),withpeak c
lationship between particle association/attachment and en- m
periods occurring in the winter and the age group at highest hanced survival (41, 45, 128, 194). Obviously, short-range r
riskbeingthose(cid:1)65yearsold(33,178).Of128studiedcases transmission (person to person) of infectious viruses such as .a
s
ofcoccidioidomycosisthatoccurredbetween1Septemberand the influenza viruses and rhinoviruses is an evolved means of m
31 December 1991 in Tulare County, CA, males, Asians and movement. Short-range atmospheric transmission via dried .o
blacks, and those over 20 years old were identified as the aerosolizedrodentexcreta(dust)istheprimaryrouteofhan- rg
highest risk groups (57). In addition to wind-generated dust tavirusinfection,andelevatedriskhasbeendocumentedinthe /
o
storms, an outbreak of coccidioidomycosis resulting in 203 aridAmericansouthwestduringdroughtsthatfollowElNin˜o n

casesandthreefatalitiesfollowedexposurefromearthquake- events(59).Evidenceoflonger-rangetransmission(buildingto J
a
generateddustclouds(208).Between1991and1993,medical building) of the severe acute respiratory syndrome virus has n
expensesassociatedwithoutbreakswereestimatedat$66mil- been documented (262), but what about even longer-range ua
lion(113). transmission? Is there a range limit with various human viral ry
Whilenootherfungaloutbreaksinhumanpopulationshave pathogensthataretransmittedthroughtheair?Howdoesthe 1
beenattributedtoduststormexposure,thecitedfungalprev- limit vary between viral pathogens, and what is the evidence 2,

alence studies in desert soils and dust storms have demon- thatlong-rangetransmissionoccurs? 2
0
strateddiversecommunitiescomposedofbothnonpathogenic Inlivestockpopulations,duststormshavebeenidentifiedas 1
and pathogenic genera and species. In most of these studies, a possible source of foot-and-mouth disease virus outbreaks 9
b
onlyafractionoftheobservedculturablecommunitywasiden- that occurred in Korea and Japan. Some of the outbreaks y
tified, or the methods employed for identification, such as followed Gobi/Takla Makan dust events (115, 175, 203). Al- g
u
morphological or spore identification, limited the ability to though two studies (115, 175) screened dust samples for the e
identifypathogenicspecies.Asaresult,researchhasproduced presenceoffoot-and-mouthdiseasevirusbyreversetranscrip- s
t
only an indication of the true community structure in any of tasePCR((cid:5)400samples)withnopositiveresults,theauthors
thedustsourceregions.Whiletheyhaveyettobeidentifiedin suggestedadditionaltestingbeforerulingoutthetransmission
duststormstudies,fungalpathogenssuchasHistoplasmacap- route. Griffin et al. hypothesized that foot-and-mouth disease
sulatum,thecausativeagentofhistoplasmosis,oftenassociated virusoutbreaksinEuropecouldresultfromlong-rangetrans-
withexposuretodustoriginatingfromdriedbirdorbatfeces, mission in African dust based on the similarity of endemic
arecertainlyapotentialriskfactor(31,164).Table3liststhe (Africa) and outbreak serotypes, dust events and outbreak
dust storm studies in which fungal CFU or spores have been occurrences, and a favorable atmospheric route (over water)
identified, the genera known to contain pathogenic species, (81). Evidence of regional (European) airborne transmission
and,whereinformationwasavailable,thepathogenicspecies. offoot-and-mouthdiseasevirustodownwindlocationswithin
Informationavailableonthesegeneraindicatesthatmostare theUnitedKingdom,fromFranceacrosstheEnglishChannel
cosmopolitan in nature. These pathogenic or opportunistic totheUnitedKingdom,andfromGermanyovertheBalticSea
pathogensareknowntocauseawiderangeofhumandiseases to Denmark, has been well documented (51, 69, 71, 72, 157,
(mild to fatal disseminating infections). Some of the fungi in 217). Using an atmospheric model and inputting optimal cli-
Table 3 are known to be mild or potent allergens (species of mateandtopography,Sorensenetal.estimatedthat1,000pigs
468 GRIFFIN CLIN.MICROBIOL.REV.
TABLE 3. Fungicapableofaffectinghumansa
Organism Location(s)(reference(cid:10)s(cid:11))b Dustsourceregion(s) Miscellaneousinformationc Disease(s)d
Acremonium USVI,Turkey(82,83) Sahara/Sahel, Commoninsoil,onplants, Mycetoma(colonizationof
MiddleEast andindoors tissue/bone),onychomycosis
(colonizationofnail),
mycotickeratitis,anumber
ofdifferentallergen-related
diseasetypesinthe
immunocompromised
Alternaria Mali,Africa,mid-Atlantic, Sahara/Sahel,Gobi/ Commoninsoil,onplants, Cutaneousphaeohyphomycosis
Barbados,Taiwan,Saudi TaklaMakan, andindoors (colonizationofskin),potent
Arabia,Israel,Turkey MiddleEast allergen(commoncauseof
(82,83,92,117,126,190, extrinsicasthma)-related
207,256) disease,deeptissueinfections
intheimmunocompromised
D
Alternariainfectoria Turkey(82) Sahara Commonenvironmental Phaeohyphomycosis
o
isolate w
Arthrinium Barbados(190) Sahara/Sahel Commonenvironmental Allergen-relateddisease n
isolate lo
Aspergillus Mali,Africa,USVI, Sahara/Sahel,Gobi/ Commoninsoil,organic Aspergillosis(pulmonary a
Barbados,Taiwan,Saudi TaklaMakan, detritus,andindoors (cid:10)allergicandcolonizing(cid:11), d
e
Arabia,Israel(79,83,92, SaudiArabia disseminated,centralnervous d
117,126,207) system,cutaneous,nasal- f
r
orbital,andiatrogenic),a o
numberofdifferentallergen- m
relateddiseasetypesinthe h
immunocompromised t
t
Aspergillusclavatus Barbados(190) Sahara/Sahel Commonenvironmental Invasiveaspergillosis p
:
isolate //
c
Aspergillusflavus Barbados,Israel(190,207) Sahara/Sahel Commonenvironmental Invasiveaspergillosis m
isolate
r
Aspergillus Barbados,Israel(190,207) Sahara/Sahel Commonenvironmental Invasiveaspergillosis .a
fumigatus isolate s
m
Aspergillusniger Mali,Africa,Barbados, Sahara/Sahel Commonenvironmental Invasiveaspergillosis
Israel(117,190,207) isolate .o
Aspergillusterreus Barbados(190) Sahara/Sahel Commonenvironmental Invasiveaspergillosis rg
isolate /

Aspergillusustus Israel(207) Saharan Commonenvironmental Rare,invasiveaspergillosis o
n
isolate
J
Aspergillus Mali,Africa,Israel(117, Sahara/Sahel Commonenvironmental Invasiveaspergillosis a
versicolor 207) isolate n
Aureobasidium Mid-Atlantic,USVI(79, Sahara/Sahel Distributedintemperate Cutaneousphaeohyphomycosis, u
a
83) areas;commononplant invasivediseaseinthe r
tissueandindoors immunocompromised y

Bipolaris USVI(79) Sahara/Sahel Commonplantandindoor Pansinusitis, 1
2
isolate meningoencephalitis,chronic ,

pulmonarydisease 2
Cladosporium Mali,Africa,mid-Atlantic, Sahara/Sahel,Gobi/ Mostcommonlyisolated Cutaneousphaeohyphomycosis, 0
1
USVI,Barbados,Taiwan, TaklaMakan, fungusinoutdoor chromoblastomycosis 9
SaudiArabia,Turkey MiddleEast studies (subcutaneousskin b
(78,79,82,83,92,117, infections),mycotickeratitis, y
126,256) potentallergen-related g
disease u
e
Cladosporium Mali,Africa,USVI,Israel Sahara/Sahel Commonenvironmental Cutaneousphaeohyphomycosis, s
cladosporioides (78,117,207) isolate chromoblastomycosis t
Cladosporium Israel(207) Sahara Commonenvironmental Cutaneousphaeohyphomycosis,
sphaerospermum isolate chromoblastomycosis
Chrysosporium USVI(79) Sahara/Sahel Commonenvironmental Opportunistic,infectingbrain,
isolate nasalandskintissue
Curvularia Taiwan,Barbados(92) Gobi/TaklaMakan Commonenvironmental Allergen-relateddisease,
isolate opportunistic,pneumonia,
disseminated
Emericellanidulans Mid-Atlantic(83) Sahara/Sahel Commonintropicaland Allergicalveolitis
subtropicalenvironments
Fusarium Taiwan,Turkey(82,92, Gobi/TaklaMakan, Commonsoilandindoor Invasivecutaneous
256) MiddleEast isolate (erythematouslesionsand
nodules),systemic
granulomatousdisease,
allergen-relateddisease
Microsporum USVI,Turkey(79,82) Sahara/Sahel, Somespeciesare Dermatophytosis(i.e.,
MiddleEast geographicallyrestricted ringworm)
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