Encyclopedia of bioterrorism defense

631 Pages·2011·82.339 MB·English

by  Rebecca Katz, Raymond A Zilinskas

ABUSAYYAF GROUP (ASG) ArticleContents
JOHNJ.RYAN • Introduction
• History
• Ideology
• CurrentStatus
• SelectedChronology
• Implications
• References
INTRODUCTION whereitstillthrivestheretoday.TheestablishedMuslim
populationresistedSpanishcolonizers,suchasFerdinand
The Abu Sayyaf Group (ASG; Arabic for ‘‘bearer of the Magellan,whospreadChristianitythroughoutthePhilip-
sword’’ or, more literally, ‘‘father of the swordsman’’) is pines. Today Roman Catholicism is the predominant
a Filipino Muslim terrorist group that seeksto create an religioninthe island nation and followersof Islammake
Islamic state in the Southern Philippines. The ASG was up a small minority. The Treaty of Paris ended the
established by Abdurajak Abubakar Janjalani between Spanish–American war and ceded control of the Philip-
1989 and 1992. The closest person ASG has to a leader pinestotheUnitedStatesin1898.FutureU.S.President
is Radullan Sahiron, and its strength is estimated to be WilliamHowardTaftbeganguidingtheFilipinostoward
between 200 and 500 members. The ASG shares close independence as governor general in 1900, and they
ties with the more radical elements of Jemaah Islamiya finally realized independence after World War II (WWII)
(JI),theMoroNationalLiberationFront(MNLF),andthe byactoftheU.S.Congressin1946(Guillermo,2005).
MoroIslamicLiberationFront(MILF)andhasbeenlinked Sinceitsindependence,thePhilippineshasfacedboth
to al-Qa’ida as well as other Middle Eastern terrorist Communist and Muslin insurgencies in its southern
organizations. provinces (Guillermo, 2005). The MNLF, a Muslim
Since its formation, the ASG has shifted between insurgent group seeking an independent Muslim nation
functioning as a terrorist organization and as a crimi- intheSouthernPhilippines,continuestofightagainstthe
nal syndicate. The ASG originally received funding from Filipino government today. It has spawned more radical
likemindedterroristorganizationsthroughouttheMiddle Islamic groups that are more willing to use terrorist
East and from the International Islamic Relief Organi- tactics in their pursuit of an independent Muslin state.
zation (IIRO). Foreign funding for the group has largely The MILF broke away from the MNLF in 1977 after
driedupduringtheinternationalWaronTerror.TheASG the MNLF signed the 1976 Tripoli Agreement with the
hasresortedtocriminalactivities,suchaskidnapforran- central government. The Tripoli Agreement granted the
som, to acquire funds (Pinkowski, 2008). The group has MNLFanautonomousregionintheSouthernPhilippines
attackedChristianmissionaries,tourists,andPhilippines ratherthananindependentstate.
governmentofficials. The ASG was formed sometime between 1989 and
The ASG operates in Basilan, Sulu, Tawi-Tawi, Zam- 1992.ManymemberswereformermembersoftheMNLF
boanga, Southern Mindanao, and occasionally in Manila and the MILF. ASG’s initial membership was made up
and Malaysia. The group seeks to establish an Islamic of the more radical members of those groups’ and was
stateinthepredominantlyMoro(FilipinoMuslim)areasof led by Abdurajak Abubakar Janjalani, a veteran of the
theSouthernPhilippinesandMalaysia.Thisareaincludes mujahidin’sfightagainsttheSoviet’sinAfghanistan.Jan-
theSuluarchipelago,WesternMindanao,SouthernThai- jalani named his organization after Abdul Rasul Sayyaf,
land,andBorneo.MembersoftheAGSarewillingtouse whowashismujahidincommanderinAfghanistan.Sayyaf
violenceagainstciviliansandgovernmentforcestoattain followedastrictinterpretationofIslamcalledWahhabism,
their goals. Since the beginning of the War on Terror in which had a great influence on Janjalani (Lehr, 2007).
2001, the Armed Forces of the Philippines (AFP) have After studying in Saudi Arabia and Libya, Janjalani
received assistance from the U.S. military and have had formed the Moro Commando Freedom Fighters (MFCC)
great success against the ASG, diminishing its member- in1990;someconsiderthisgrouptobethepredecessorof
shipbytwothirds. thecurrentASG.
Janjalani reportedly received funds from Muhammad
JamalKhalifathroughtheIIROtostarttheASG.Khalifa
HISTORY is a brother-in-law of Osama bin Laden and a member
of the Muslim Brotherhood. The first attributable attack
Arab traders brought Islam to the Southern Philippines by the ASG was perpetrated in 1991 against Christian
in the 13th century. It spread throughout the Sulu missionaries aboard the ship M/V Doulos in the port of
archipelago and to the southern region of Mindanao, Zamboanga.In1995,theASGwaslinkedtoRamziAhmed
EncyclopediaofBioterrorismDefense,2ndEdition, EditedbyRebeccaKatzandRaymondA.Zilinskas
Copyright©2011JohnWiley&Sons,Inc.
1
2 ABUSAYYAFGROUP(ASG)
Yousef’s Bojinka plot. Yousef had been the mastermind theferry.KhadaffyalsodevelopedclosetieswithJIoper-
behind the 1993 World Trade Center bombing in New atives and radical members of the MILF. Khadaffy was
York City. His Bojinka plot was an elaborate scheme to killedinSeptember2006duringafirefightwiththeAFP.
assassinate both Pope John Paul II and President Bill TheAFPalsokilledhislikelysuccessor,AbuSulaiman,on
Clinton while they were in the Philippines, fly a plane JoloIslandinMarch2007.However,thelossofitstwotop
into the Central Intelligence Agency (CIA) headquarters leadershasnotstoppedtheASG.ABasilanCongressman
in Langley, VA, and blow up a dozen airlines over the who was a former member of the ASG and an outspoken
Pacific Ocean. The plot was broken up by Filipino police critic of the group was assassinated by an ASG bomb in
beforeanyattacktookplace. November2007(Lehr,2007).
Janjalani was killed by the AFP in 1998. After his
death, his younger brother Khadaffy Janjalani and Abu
Sabaya (also known as Aldam Tilao) took control of the IDEOLOGY
groupinBasilan.ThegrouponJoloIslandcontinuedtobe
led by Galib Andang (also known as Commander Robot). The Abu Sayyaf Group was founded to build upon the
However, the death of the elder Janjalani factionalized goals of the MNLF and the MILF, namely to create an
the ASG. The ASG devolved into a criminal group that Islamic state in the Southern Philippines governed by
focused on for-profit crimes, such as kidnap for ransom. the Sunnah of Mohammad. The ASG’s founder, Abdu-
AfterabductingEuropeancitizensin2000,millionsofdol- rajak Abubakar Janjalani, believed that an independent
larswerefunneledfromEuropeangovernments,through Islamic state was necessary because of the oppression of
Muammar al-Qadhafi’s Libyan government, to the ASG theMoro(FilipinoMuslim)peoplebythePhilippinesgov-
kidnapperstowinthehostages’release.Alsoin2000,the ernment and that violence was justified in attaining an
ASGkidnappedseveraltouristsfromaresortonPalawan. independentstate(Lehr,2007).Janjalanihadbeeninflu-
OneAmericantouristwasbeheaded.TwoAmericansand enced by Abdul Rasul Sayyaf, a strict Wahhabi, during
a Filipino remained hostages when the AFP, aided by histimeinAfghanistanfightingtheSovietoccupation.In
U.S. Special Forces, attempted a rescue in June 2002. 1998, the Abu Sayyaf Group committed itself to Osama
During the rescue attempt, the Filipino and an Ameri- bin Laden and to Ayman al-Zawahiri’s fatwa under the
can hostage were killed, and only one American hostage banner of ‘‘The World Islamic Front for Jihad Against
wassuccessfullyrescued.Morethananyother,thisevent Jews and Crusaders,’’ which called for Muslims around
broughttheASGtotheattentionoftheU.S.government the world to kill U.S. citizens, civilian and military, and
(Linden,2004). theirallieseverywhere(Pinkowski,2008).
Philippines President Gloria Macapagal–Arroyo
stronglysupportedtheUnitedStatesafter9/11initsWar
CURRENTSTATUS
on Terror. Arroyo allowed Filipino military bases to be
used by U.S. forces to invade Afghanistan. In turn, U.S.
TheASGcontinuestooperateintheSouthernPhilippines
forces begantraining and equipping the AFPto fight the
andhasbetween200and500members.Thegroupisactive
ASG more effectively. In January 2002, 650 U.S. Special
in Basilan, Sulu, Zamboanga City, Zulu, and Tawi-Tawi.
Forces and support troops were deployed to Mindanao
The ASG has strengthened ties with the most radical
and Basilan (Linden, 2004). U.S. and Filipino forces
members of JI, and it continues to perpetrate terrorist
also conducted joint military exercises called Balikatan,
attacks.However,thegroupsuffersfromalackofdecisive
which means‘‘shouldering the loadtogether.’’U.S.forces
leadership.Thereiscurrentlynoclearleader.Commander
are prevented from directly engaging the ASG by the
Radullan Sahiron is said to be the de facto leader of the
Filipinoconstitution,butAFPoperationshavediminished
ASG.YasserIgasanhasalsobeenmentionedasapossible
the ASG’s strength to one third of what it once was.
leader. The ASG forces are split into cells on various
The Australian government also funds counterterrorism
islands that are led by individual commanders rather
programs that target the ASG through the Philippine
than by an overall leader. The ASG lacks organization,
National Police (PNP). However, Filipino laws have not
a coherent strategy, and funding, which has caused it to
caught up with the military, and some terrorists have
devolveyetagainintoalargekidnapforransomoperation.
been released because of a lack of laws governing their
TheAFPannouncedinJuly2009thatitwoulddefeatthe
actions. The Human Security Act, passed in July 2007,
ASGbytheendoftheyear.
was enacted to make it easier for the Filipino judicial
system to combat terrorism. However, it has only been
usedoncesinceitsenactmentbecauseitplacesafinancial
SELECTEDCHRONOLOGY
compensation burden on individual officers rather than
onthePNPifasuspectisfoundnotguilty.
Table1listscrimescommittedbytheASGbetween1991
In 2003, Khadaffy began reorienting the ASG away
andJuly2009.
fromitscrime-for-profitmentalitybacktowarditsoriginal
ideologicalrootsandcrimeforpoliticalgain.InFebruary
IntenttoAcquireandUseBiologicalWeaponsandOther
2004, the ASGattacked and sank the MVSuperferry 14,
WeaponsofMassDestruction(WMD)
which had almost 900 people onboard. The attack killed
morethan100peopleandinjuredmorethan300.TheASG As of summer 2008 the ASG has not made any public
allegedlyused 8lbs ofTNT hiddeninatelevisionto sink statements showing an interest in chemical, biological,
ABUSAYYAFGROUP(ASG) 3
Table1. ChronologyofCrimesCommittedbyAbuSayyafGroup1991–2009
Date Location Event
August,1991 Philippines GrenadekilledtwoChristianmissionariesaboardtheM/VDouloswhiledockedinthe
portofZamboanga;AbuSayyafGroupsuspected.
May20,1992 Philippines ItalianmissionaryassassinatedinZamboangaCity;AbuSayyafGroupsuspected.
April,1995 Philippines AbuSayyafGroupforcesraidedthetownofIpilinMindanao.
April,2000 Philippines AnAbuSayyafGroupfactionkidnapped21peopleincludingWesterntouristsfroma
Malaysianresort.
December30,2000 Philippines SeriesofbombsinManilakilled16andinjuresatleast30;AbuSayyafGroup
suspected.
May27,2001 Philippines AbuSayyafGroupkidnapped3Americansand17FilipinosfromaresortinPalawan.
SeveralFilipinohostageswereexecutedandanAmericanwasbeheaded.Duringa
rescueattemptbytheAFPonJune7,2002,oneAmericanwasrescuedandone
AmericanandoneFilipinowerekilled.
October,2002 Philippines AU.S.servicemanwaskilledwhenanAbuSayyafGroupbombexplodedneara
FilipinomilitarybaseinZamboanga.
February27,2004 Philippines AbuSayyafGroupbombedtheSuperferry14inManilaBay,killing116people.
March,2004 Philippines AnAbuSayyafcellwasbrokenupbyFilipinoauthorities.Theyhadplannedtoattack
theU.S.EmbassyinManila.
February14,2005 Philippines BombsexplodedinManila,DavaoCity,andGeneralSantosCity,killing8andinjuring
morethan150people.TheAbuSayyafGroupclaimedresponsibility.
January,2007 Philippines ThreesimultaneousattackstookplaceonsiteshostingtheAssociationofSoutheast
AsianNations(ASEAN)andEastAsianregionalsummits.TheAbuSayyafgroup
wassuspected.
July,2007 Philippines AbuSayyafGroupandMILFforcesengagedtheAFPonBasilanIslandandkilled14
membersoftheAFP,beheading10ofthem.
November,2007 Philippines AmotorcyclebombexplodedoutsidethePhilippinesCongress,killingacongressman
andthreestaffers.
February,2008 Philippines AnAbuSayyafGroupplottoassassinatePresidentArroyowasdisrupted.
May29,2008 Philippines AbombexplodedatanairforcefacilityinZamboanga.TheAbuSayyafGroupwas
suspected.
January,2009 Philippines ThreeRedCrossofficialswerekidnappedbyAbuSayyafGroup.
July7,2009 Philippines AcommercialareaonJoloIslandandamilitaryjeepinIlliganCitywerebombed.
AnotherbombwasfoundanddisarmedataCatholiccathedralonJoloIsland.The
AbuSayyafGroupwasstronglysuspected.
radiological, or nuclear (CBRN) weapons. The ASG cer- commitcrimesforprofit, such askidnapping forransom,
tainly is not capable of developing a CBRN capability on rather than politically motivated acts of terrorism. Nei-
itsown,anditisnotbelievedthattheASGhasattempted ther the ASG nor the terrorist groups that it has close
toacquiretheseweaponsthroughathirdparty.Thenec- ties with possess a CBRN capability, and the ASG can-
essaryeducationandfacilitiestodevelopCBRNweapons not develop a CBRN capability on its own. Furthermore,
do not exist in the ASG’s area of operation. It is unlikely the ASG has expressed no interest in attaining or using
that the ASG would use aCBRN weaponeven if it could a CBRN weapon, so it is very unlikely that they would
becausetheareawhereitoperatesisalsowhereitseeksto commitaCBRNattack.
establishanindependentIslamicstateandderivesitspop-
ularsupport.TheASGdoeshaveclosetiestobothJIand
al-Qa’ida, two groups that have actively sought a CBRN REFERENCES
capability,butneithergroupisbelievedtohavedeveloped
CBRN weapons to date, and the ASG has expressed no Guillermo, A.R., The Historical Dictionary of the Philippines:
interestinaCBRNcapability. SecondEdition,TheScarecrowPressInc.,Lanham,MD,2005.
Lehr,P.,ViolenceatSea:PiracyintheAgeofGlobalTerrorism,
Routledge,NewYork,2007.
IMPLICATIONS
Linden, E.V., Foreign Terrorist Organizations: History Tactics
and Connections, Nova Science Publishers Inc., New York,
Although the AFP has severely diminished the numbers
2004.
andcapabilitiesoftheASG,AbuSayyafGroupwilllikely
Pinkowski, J., Homeland Security Handbook, CRC Press, New
continue itssmall-scale terroristattacksand itscriminal
York,2008.
activity.Becauseofthelackofoutsidefunding,thecrim-
inal activity is necessary for the ASG to assemble funds
with which to pursue its ideological goals. With pressure FURTHERREADING
from the AFP and a lack of outside resources, the ASG Burnham, G. In the Presence of My Enemies, Tyndale House
couldcontinuetodevolveintorovinggangsofbanditswho Publishers,CarolStream,IL,2003.
4 ABUSAYYAFGROUP(ASG)
Manalo, E.P., The Philippine Response to Terrorism: The Abu StudyofTerrorismandResponsetoTerrorism(START),http://
SayyafGroup,StormingMedia,Washington,DC,2004. www.start.umd.edu/start/data/tops/terrorist_organization_
profile.asp?id=204.
WEBRESOURCES
Council on Foreign Relations, http://www.cfr.org/publication/
9235/abu_sayyaf_group_philippines_islamist_separatists. See also AL-QA’IDA, JEMAH ISLAMIYAH, and MORO ISLAMIC
html. LIBERATIONFRONT.
AEROSOL (AEROBIOLOGY, AEROSOLS, BIOAEROSOLS, MICROBIAL ArticleContents
AEROSOLS)
• Introduction
• Background
ALLENJEFFMOHR
• TechnicalReview
• PhysicalParameters
• BiologicalParameters
• InactivationMechanisms
• CurrentIssues
• References
INTRODUCTION be explained by the varied methodologies employed to
study the subject. The results of aerosol stability studies
Aerobiology is the study of microbiological particles that are dependant on the method of microbiological sample
have, either naturally or purposefully, been introduced preparation, sample storage, and sample quantification.
into the air. The science of bioaerosols is extremely com- Additionally, the results are dependent on the type of
plex, and to understand the subject fully, it is necessary aerosol aging drum used, the methods of aerosol gen-
to have an understanding of microbiology, meteorology, eration and sampling, and the types of fluids used for
biochemistry, and aerosol physics. Bioaerosols are usu- suspension and collection. Because of the recent interest
ally presented as polydispersed particles or droplets and in bioterrorism, the science of aerobiology has become a
rangeinsizefrom0.5to15.0micrometers(μm).Theopti- topic that is receiving renewed attention. Authoritative
mal aerodynamic particle size range, which represents a texts and up-to-date advances will be discussed later in
hazard to the human respiratory tract, is between 1.0 thischapter.
to about 10.0 μm. Particles between 1.0 and 3.0 μm are
typicallythemosthazardousbecausetheycanbeinhaled
TECHNICALREVIEW
intothedeepestregionsofthelungs(alveoli)andinitiate
respiratorydisease.
Thefateandtransportofbioaerosolsisacomplicatedissue
Bioaerosols of significance to terrorism include both
involvingmanyphysicalandbiochemicalfactors(Table1).
human and agricultural pathogens and toxins. These
The transport of bioaerosols is primarily governed by
aerosols can consist of spore-forming bacteria, vegetative
hydrodynamic and kinetic factors, whereas their fate
bacteria,rickettsia,viruses,toxins,andfungi.Bioaerosols
dependsontheirspecificchemicalmakeupandthemete-
areattractiveasterroristweaponsbecausetheyaresilent,
orologicalparameterstowhichtheyareexposed.Whena
invisible,odorless,andcanbeintroducedclandestinelyto
bioaerosol particle approaches a surface, the effects gov-
strikewithoutwarning.
ernedbythemakeupofthebiologicalagent’scellwallwill
influencedeposition.Specificsurface–surfaceinteractions
BACKGROUND then dictate the release of the particle (Lighthart and
Mohr,1994).
The controlled study of biological aerosols can be traced Mostairbornemicroorganismsareimmediatelyinacti-
backtotheearly1930s,whentheJapanesemilitaryinten- vateduponreleasebecauseofenvironmentalstressesthat
tionally infected prisoners with bioaerosols to determine acttoalterthemakeupoftheoutersurfaceofthemicroor-
their application in war. In 1942, the United States ini- ganism.Themostsignificantenvironmentalfactorsinflu-
tiated its offensive program to study the infectivity and encingviabilityarerelativehumidity(RH),temperature,
aerosol stability of biological agents. Between 1949 and andoxygen.Additionalinfluencesareexertedthroughair
1968, the United States studied the aerosol dispersion ions,solarirradiance,andopenairfactors(OAF).
characteristics of biological simulants when released at Bioaerosol particles can be either solid or liquid and
varioussitesinthecountry.In1998,itwasrevealedthat can come from many natural and anthropogenic sources.
theformerSovietUnionhadproducedbiologicalagentson Although few generalities can be made concerning the
a massive scale for decades and had developed methods aerosol stability or fate of microorganisms, bacteria
forweaponizinghemorrhagicfevervirusestoenhanceits tend to behave differently compared with viruses, which
BWpotential. behavedifferentlyfrommoldsandfungus.Somemicroor-
Today,fewauthoritative textsdealdirectly withaero- ganisms have built-in mechanisms that act to repair
biology because it is a comparatively new discipline and damage inflicted during the aerosolization and transport
hasnotbeencomprehensivelystudied.Resultspresented phases.
in peer-reviewed articles are often confusing, and con- High priorities have recently been placed on rapidly
tradictory resultsarecommon.Theseinconsistencies can developing biodefense capabilities. Excellent reviews
EncyclopediaofBioterrorismDefense,2ndEdition, EditedbyRebeccaKatzandRaymondA.Zilinskas
Copyright©2011JohnWiley&Sons,Inc.
1
2 AEROSOL(AEROBIOLOGY,AEROSOLS,BIOAEROSOLS,MICROBIALAEROSOLS)
Table1. FactorsAffectingtheViabilityofAirborne Temperature
Microorganisms
ThevaporpressureandthereforetheRHofasystemare
PrimaryFactors References dependent on the temperature. This relationship makes
itverydifficulttoseparatetheeffectsoftemperatureand
Humidity Coxetal.,1974
CoxandGoldberg,1972 RH. Studies to determine the effect of temperature on
Sattaretal.,1984 aerosol stability have generally shown that increases in
Theunissenetal.,1993 temperature tend to decrease the viability of airborne
Temperature Dimmock,1967 microorganisms (Dimmock, 1967). Additionally, frozen
Theunissenetal.,1993 cellstendtolosecellularproteins(namelypermease)that
Radiation Donaldson,1972 enhanceaerosolinactivationrates.AswithRH,thetargets
Jensen,1964
oftemperature-inducedinactivationseemtobemembrane
OAF deMikanddeGroot,1977
phospholipidsandproteins.
DonaldsonandFerris,1975
Druett,1973
OxygenConcentration
SecondaryFactors References
Oxygen concentration can have an important effect on
Methodofaerosolgeneration Heidelbergetal.,1997 theaerosolstabilityandinfectivityofsomebacteria(Cox
Marthietal.,1990
etal.,1973,Coxetal.,1974).Freeradicalsofoxygenhave
Seungetal.,2007
beensuggestedasacauseofinactivation.Someinvestiga-
Compositionofgenerationfluid Cox,1987
torshaveobservednegativerelationshipsbetweenoxygen
Samplingmethod MarthiandLighthart,1990;
concentration and viability. It has been shown that oxy-
Warrenetal.,1969
Seungetal.,2007 gen susceptibility increases with dehydration, increased
Hermannetal.,2006 oxygenconcentration,andtimeofexposure.Thetargetsof
Collectionmedium ElazharyandDerbyshire,1977 oxygen-inducedinactivationalsoseemtobephospholipids
andproteins.
(Phalen, 2009; Swearengen, 2006) are available that ElectromagneticRadiation
present recent efforts that encourage researchers to Aerosol inactivation caused by electromagnetic radiation
leverage relevant results rather than duplicate them. has been shown to be dependent on the wavelength and,
The most recent advances in animal model development hence,theintensityoftheradiation.Shorterwavelengths
and experimentation are aimed at developing medical contain more energy and are generally more deleterious
countermeasuresthroughabetterunderstandingofphys- to aerosolized microorganisms. The targets of radiation-
iologyandthemostcurrentappliedbioaerosolgeneration induced inactivation seem to be phospholipids, proteins,
andsamplingtechniques.Thesereferencesexaminethose andnucleicacids.Thenegativeimpactofsolarirradiance
bacterial, viral, and toxic agents considered to pose the ontheviabilityofbioaerosolscannotbeoveremphasized.
greatestthreatstopublicsafety.
BIOLOGICALPARAMETERS
PHYSICALPARAMETERS
Thetype,species,orstrainofamicroorganismwillaffect
WaterContent
its airborne survival. The atmospheric environment is
The state of water and the water content associated hostiletoallmicroorganisms;nospecieshasevolvedtofill
with bioaerosols are fundamental factors influencing thenicheoftheopenatmosphere.
the fate or viability of microorganisms. As the RH
decreases, so does the water available to the exterior
Bacteria
environment of the microorganism. A loss of water can
cause dehydration, resulting in the inactivation of many Evidence suggests that some bacteria form new cells in
microorganisms. Of all the measurable meteorological theairborne state(Dimmicketal.,1979).Gram-negative
parameters, RH is the most important with respect to bacteria contain more phospholipids than gram-positive
aerosol stability (Cox, 1987). Israeli et al., (1994) studied bacteria.Forthisreason,theyaremoresusceptibletoinac-
freeze-dried microorganisms and showed the importance tivation through such mechanisms as Maillard reactions
of water content to the viability of microorganisms. (reactionsbetweenproteinsandcarbohydrates),dehydra-
They concluded that biomembranes, as phospholipid tion,andosmoticshock.Bacteriagrownonenrichedmedia
bilayers, undergo conformation changes from crystalline displaywidelyvaryingaerosolstabilityrates,asdobacte-
to gel phases as a result of water loss. These transfor- ria in different phases of development. The physiological
mations induce changes to cell proteins, which in turn age of a bacterial population also influences its stability
result in a loss of viability. The targets of RH-induced because old cells die off at higher rates than do newly
inactivation seem to be membrane phospholipids and grown samples. Furthermore, cells grown during the log
proteins. phasemaybemoreactivemetabolically,andsomesystems
AEROSOL(AEROBIOLOGY,AEROSOLS,BIOAEROSOLS,MICROBIALAEROSOLS) 3
maybemorevulnerabletostresses,thanthoseinthesta- Fungi
tionaryphaseofgrowth.Intherecentpast,littleworkhas
Fungiandtheirsporesseemtoberesistanttodesiccation,
been completed on the aerosol stability of bacteria as it
butlittleworkhasbeencompletedinassessingtheirsur-
appliestobiologicaldefense.
vival rates in aerosols. Interest has intensified recently
Table2showssomeparametersthathavebeenshown
with the phenomenon termed ‘‘sick building syndrome’’
to influence the viability of selected bacteria. Differences
(SBS).Itisbelievedthatfungiandbacteriaareresponsi-
are not only a result of dissimilar test procedures and
ble for most SBS cases, even though most of the 100,000
data representation but also are caused by the greater
known species of fungi do not cause disease in healthy
structuralandmetaboliccomplexityofbacteria(cellwalls,
people. More common effects of the presence of fungi
membranes, and metabolism). The following generalities
in buildings are asthma, allergenic-type responses, and
canbeinferredconcerningtheaerosolstabilityofbacteria:
sometimes significant respiratory distress. Many fungi
producetoxinsthat,wheninhaledinhighconcentrations
• Lossofaerosolviabilityiscausedbydesiccationand
(as can occur with farm workers or people working in
oxygentoxicity.
granaries),canresultinsignificanthealthconsequences.
• Somegram-negativebacteriaareinactivatedbyoxy-
genafterdesiccation.
Toxins
• ManybacteriahavecomplicatedRH-inactivationpro-
filesininertatmospheres. Fewreferencesaddressthestabilityofaerosolizedtoxins.
• Bacterial survival can be greatly increased by the Because toxins are chemicals, their inactivation during
traveldownwindislessaffectedbymeteorologicalfactors
additionofstabilizers(e.g.,carbohydrates).
(desiccation caused by low RH, temperature, and solar
• Aerosolized spores of many bacteria are resistant
irradiance)thanbyviablebacteriaandviruses.Forthese
to inactivation by oxygen concentration, RH, and
reasons, the aerosol activity of toxins presumably falls
temperature.
betweenstablebacterialsporeformers(Bacillusanthracis)
and fragile vegetative bacteria (such as Yersinia pestis,
Viruses Francisellatularensis,etc.)
Table 3 lists some parameters that have been demon-
strated to influence the viability of selected viruses.
Viruses are normally very resistant to inactivation by INACTIVATIONMECHANISMS
oxygen.Becauseofthischaracteristic,andbecauseofthe
Bioaerosolsaresubjecttoinactivationduringstorage,dur-
relativesimplicityoftheirstructure,theresultsofaerosol
ingdissemination,andespeciallyduringaerosoltransport.
inactivation studies are more consistent for viruses than
Desiccation of the droplet is the main factor responsible
for bacteria. Recent interest in the Swine influenza
for inactivation (Wells, 1934). Applicable particle sizes
virus (SIV) and other viruses have revived research on
range from 0.5 to 15 μm. (Particles smaller than 5.0 μm
their viability characteristics in aerosols (see subsequent
act as vapors and follow the streamlines of the local
section). The following generalities can be made about
airstreams.) Some relationships between aerosol stabil-
aerosolinactivationratesforviruses:
ityandthebiologicalcompositionofmicroorganismshave
• Viruses with lipids in their outer coat or capsid are beenidentified.Bacterialaerosolstabilityisconsiderably
morestableatlowRHsthanathighRHs. more complex than that observed for viruses. For bacte-
• Viruses without lipids are more stable at high RHs riaaerosolizedintoinertatmospheresatmid-to-highRH,
thanatlowRHs. thebiologicalmembraneconstituentsbecomedestabilized
• When viable viruses can no longer be detected after through loss of water molecules. Additives that super-
saturate, such as polyhydroxyl compounds, can stabilize
aerosol collection, nucleic acids can be isolated and
these structures. The polyhydroxyl compounds, by bind-
are still active (this evidence suggests that aerosol
ingtositesonproteins,causeconformationalchangesand
inactivation of viruses is not caused by nucleic acid
therebystabilizetheproteins,makingthemlesssuscepti-
inactivationbutbythedenaturationofcoatproteins).
ble to denaturation. This is convincing evidence that the
• Prehumidification during sampling increases the
stateofproteinsontheoutermembraneofsomemicroor-
recovery of viruses that lack lipids in their outer
ganismsiscriticaltotheresultantstabilityprofile.
coat.
Cox’s(1987)explanationofthesequenceofeventsisas
It is also interesting to note that some viruses exhibit follows. There is little doubt that during the desiccation
highersurvivalratesatmidrangeRH,regardlessoftem- process, polyhydroxyl compounds and amino acids react
perature,whereassomevirusesdisplaybettersurvivalat together,causingconformationalchangesthatstrengthen
low and high RH and the lowest survival at midrange theoverallproteinstructure.Thepresenceofsugaraddi-
RH. However, survival may depend on the temperature tivescauses conformational changes in the coat proteins,
and oxygen content of the test atmosphere at the time of and in the new configuration, these coat proteins do not
testing.Somevirusesarestableintheairbornestateover react(orreactmoreslowly)withthepolyhydroxylcoatmoi-
broadtemperatureandRHranges. eties.Intheabsenceofsugaradditivesandfreemolecules,
4 AEROSOL(AEROBIOLOGY,AEROSOLS,BIOAEROSOLS,MICROBIALAEROSOLS)
thecoatproteinsmayreactirreversibly,throughMaillard The energy applied to aerosolize dry particles may
reactions,withthepolyhydroxylcoatmoietiesandcausea come in the form of pressurized air, scraping a dried
lossofviability.Inaddition,thesugaradditivescouldcom- cake and then applying air, or employing an explosive
pete with the polyhydroxyl coat moieties for the reaction device. Bioaerosols that are initially disseminated from
sites of the coat proteins or physically hinder those reac- drypreparationsareoftenveryelectrostatic;thatis,elec-
tions’ molecular collisions. The result in each case would tricallychargedparticleswillbeattractedtooneanother
bemoreaerostablemicroorganisms. andthusformlargeclumps.
Several significant issues must be overcome to dis-
seminate infectious bioaerosols successfully. It is true
CURRENTISSUES
thatunsophisticatedmethods(agriculturalsprayers,com-
mercial aerosol devices, etc.) can be used to produce
Dissemination
bioaerosols, but the results will almost certainly be just
Thephysicalpropertiesofbioaerosolsareprimarilydepen-
as basic as the method of delivery. To produce infec-
dent on the generation method applied. Two of the most
tiousbioaerosolsefficientlyandconsistentlyinthe1.0-to
importantvariables,particlesizedistributionandconcen- 10.0-μmsizerange,acommittedtestingprogramwouldbe
tration, are directly related to the aerosolgenerator. The
requiredtoverifyinfectivityandpathogenicityaswellas
most efficient particle sizes for deposition in the human
particlesizerange.Problemsthatwouldhavetobeover-
respiratorytractliebetween1.0and10.0μm.
come include inactivation caused by the dissemination
Biological aerosols are usually produced from a liquid
system,athoroughknowledgeofappropriatemeteorologi-
suspension. Most bioaerosols generated from liquids are
calparameters,biologicalparticlestabilizers,andclogging
polydispersed in nature. The energy required to produce
ofnozzles.Theuseofsporeswouldprecludemanyofthese
small particles can come from pressurized air, electric-
concerns.
ity, centrifugal forces, impaction, or heat. Many of these
forces are so violent that inactivation of microorganisms,
Sampling
especially vegetative bacterial cells, can result. Fluid
associated with newly aerosolized particles will instan- A significant part of the science of aerobiology has been
taneously start to evaporate, and equilibrium with the directedtowardthedevelopmentofsamplersthatcollecta
surrounding watervaporwillbeestablished,resultingin representativeparcelofairwhilestrivingtominimizethe
adehydratedsolidparticle. stressesthatcauseinactivationofthetarget.Aerosolized
Table2. AerosolStabilityParametersforSelectedBacteria
Bacteria StabilityParameters References
Bacillussubtilis Deathrate Webb,1959,1960
Bacilluspatchiness Ambienttemperature,bacterialviability Webb,1959,1960
Bacillusviolaceous Ambienttemperature,bacterialviability Webb,1959,1960
Chlamydiapneumoniae RH,temperature Warrenetal.,1969
Erwiniaherbicola RH,temperature Marthi,1994
Escherichiacoli RH,temperature,O2,wet,dry Cox,1966,1968
Mycoplasmapneumoniae RH,temperature,solar Israelietal.,1994
Pasteurella(Francisella)tularensis RH,wetanddrygeneration,solar CoxandGoldberg,1972
Serratiamarcescens RH,O2,freeze,time Coxetal.,1973,1974
Staphylococcusalbus Time,ambienttemperature Webb,1959,1960
Staphylococcusaureus RH,temperature —
Table3. AerosolStabilityParametersforSelectedViruses
Virus StabilityParameters References
Footandmouthdiseasevirus Radiation,RH,temperature,weatherfactor Barlow,1972
Influenzaviruses RH Looslietal.,1943
MillerandArtenstein,1966
Newcastlediseasevirus RH,temperature Songer,1966
Pigeonpox RH,inositol Webbetal.,1963
Porcinecoronavirus RH,sampling Seungetal.,2007
PorcineReproductiveandRespiratory RH,sampling Hermannetal.,2007
SyndromeVirus
Rousesarcomavirus RH,inositol Webbetal.,1963
St.Louisencephalitisvirus RH,temperature Rabeyetal.,1969
Swineinfluenzavirus RH,sampling Hermannetal.,2007
Venezuelanequineencephalitisvirus RH,temperature,solar Dimmicketal.,1979
Vesicularstomatitisvirus RH,temperature,O3 Donaldson,1972Songer,1966
Yellowfevervirus RH,temperature MarthiandLighthart,1990
AEROSOL(AEROBIOLOGY,AEROSOLS,BIOAEROSOLS,MICROBIALAEROSOLS) 5
biologicalparticlescanbecollectedonagarsurfaces(slit- Cox,C.S.,Baxter,J.,andMaidment,B.J.,J.Gen.Microbiol.,75,
to-agarsamplers)orintobufferedliquidmedia(impinger, 179–185(1973).
cyclone,etc.).Biologicalparticlescollectedontofiltersare Cox, C.S., Gagen, S.J., and Baxter, J., Can. J. Microbiol., 20,
often inactivated owing to the severe drying affects of 1529–1534(1974).
the procedure. Liquid cyclone samplers are among the deMik,G.anddeGroot,I.,J.Hyg.,78,175–180(1977).
best collectors because they are efficient and minimize Dimmick,R.L.,Wolochow,H.,andChatigny,M.A.,Appl.Environ.
biological inactivation. Currently, no biological sampler Microbiol.,37,924–927(1979).
isavailablethatishighlyefficient,collectsisokinetically, Dimmock,N.L.,Virology,31,338–353(1967).
andmaintainsahighdegreeofviability.
Donaldson,A.I.,Vet.Bull.,48,83–94(1972).
Donaldson, A.I. and Ferris, N.P., J. Hyg. (Camb.), 74, 409–415
FutureOutlook
(1975).
Techniquesemployedtoproduce,concentrate,purify,and Druett,H.A.,‘‘TheOpen AirFactor,’’inJ.F.Ph.Hers andK.C.
storemicroorganismshavechangedlittlesincethe1950s. Winkler, Eds., Airborne Transmission and Infection, Wiley,
Additionally, little recent advancement has been made NewYork,1973,pp.141–151.
concerning the procedures used to dry, mill, weaponize, Elazhary,M.A.S.Y.andDerbyshire,J.B.,Can.J.Comp.Med.,43,
and disseminate biological agents. It is probable that 158–167(1977).
biotechnology and genetic engineering could perhaps be Heidelberg,J.F.,Shahamat,M.,Levin,M.,Rahman,I.,Stelma,
applied to affect the aerosol stability of microorganisms G.,andColwell,R.R.,Appl.Environ.Microbiol.,63,3585–3588
and toxins, but the research required to accomplish this (1997).
taskwouldbesubstantialandtimeconsuming.Advance- Hermann, J.R., Hoff, S.J., Yoon, K.J., Burkhardt, A.C., Evans,
mentsinpolymerscienceandmicroencapsulationtechnol- R.B., and Zimmerman, J.J., Appl. Environ. Microbiol., 72,
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particle, which would act to prolong the aerosol stability Israeli,E.,Gitelman,J.,andLighthart,B.,‘‘DeathMechanismsin
and hence the infective nature the biological particle. Bioaerosols,’’inB.LighthartandA.J.Mohr,Eds.,Atmospheric
One of the greatest challenges for researchers is the Microbial Aerosols, Chapman & Hall, New York, 1994, pp.
166–191.
lackofappropriateequipmenttostudytheaerosolstabil-
ity of microorganisms. Fully characterized, high contain- Jensen,M.M.,Appl.Microbiol.,12,412–418(1964).
mentrotatingdrumsneedtobedesignedandconstructed Lighthart, B. and Mohr, A.J., Atmospheric Microbial Aerosols.
to determine the inactivation characteristics of airborne TheoryandApplications,Chapman&Hall,NewYork,1994.
select agents. These new designs would require appro- Loosli,C.G.,Lemon,H.M.,Robertson,O.H.,andAppel,E.,Proc.
priate animal exposure compartments so that infectivity Soc.Exp.Biol.Med.,53,205–206(1943).
could be determined. Swearengen (2008) presents the MarthiB.,‘‘RecitationofMicrobialBioaerosols,’’inB.Lighthart
mostup-to-datereviewofthecurrentlyusedstabilityand andA.J.Mohr,Eds.,AtmosphericMicrobialAerosols,Chapman
exposure chambers, but few recent upgrades have been &Hall,NewYork,1994,pp.192–225.
developed. Marthi, B., Fieland, V.P., Walter, M., and Seidler, R.J., Appl.
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or crude methods. Techniques required to produce dry Marthi, B. and Lighthart, B., Appl. Environ. Microbiol., 56,
spore preparations are simple, but years of work were 1286–1289(1990).
requiredtodevelopthoseprocedures.Liquidsuspensions Miller,W.S.andArtenstein,M.S.,Proc.Soc.Exp.Biol.Med.,123,
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abiologicalaerosoleffort,itwouldbenecessarytohavea orpe,V.S.,Appl.Environ.Microbiol.,47,879–881(1984).
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FURTHERREADING Willeke,K.andBarons,P.A.,AerosolMeasurement,VanNostrand
Reinhold,NewYork,1993.
Dimmick,R.L.andAkers,A.B.,AnIntroductiontoExperimental
Aerobiology,Wiley-Interscience,NewYork,1969.
Fuchs,N.A.,TheMechanicsofAerosols,DoverPublications,New SeealsoPATHOGENSCAUSINGVIRALHEMORRHAGICFEVERS,UNIT
York,1964. 731,andNATIONSOFCONCERN.