FEATURE

Remediating anthrax-contaminated sites:Learning from the pastto protect the future

By Dorothy A. Canter

INTRODUCTION

Attacks with bioterrorism agents differfrom attacks using chemical or explo-sive agents in a number of importantways. First, unless reliable biologicaldetection systems have been installedat the sites, it is highly unlikely that thebioagents will be detected at the time ofattack; they will be identified only afterexposed persons become ill and visithospital emergency rooms. Hence, ter-rorists could attack multiple facilitiesbefore the first attack was detected.For example, a terrorist could releaseanthrax spores at an international air-port on the East Coast of the U.S. onMonday, then fly to a central airporthub and release more spores on Tues-day, and continue on to the West Coastto release spores at a third internationalairport later in the week. All threeattacks could take place before anyoneknew that the first had occurred. Theability to mount multiple attacks with-out promptly alerting the relevantauthorities and having them hardenother facilities to decrease the probabil-ity of further successful attacks isknown as ‘‘reload capacity’’ and is akey property of bioterrorism agents.1

Dorothy A. Canter, Ph.D., is affiliatedwith US Environmental ProtectionAgency, Washington DC, USA. Tel.:+202 566 0176; fax: +202 566 0176(e-mail: canter.Dorothy@epamail.epa.gov).

The views expressed in this paper arethose of the author and do not neces-sarily reflect those of the U.S. Environ-mental Protection Agency.

1074-9098/$30.00

doi:10.1016/j.chs.2004.12.001

Second, certain diseases caused bybioterrorism agents, such as smallpoxand pneumonic plague are not onlyinfectious, but contagious as well. Theyare spread by person-to-person trans-mission. A recent example of such anagent is the SARS virus, which spreadrapidly throughout the globe in 2003.

Third, virtually no established guide-lines exist for decontaminating sitesstruck with bioterrorism agents. Priorto the 2001 anthrax attacks, there wasvirtually no experience in, and littleplanning for, responding to attacks withsuch agents in civilian settings. TheU.S. Environmental Protection Agency(EPA) had extensive expertise inresponding to releases of toxic indus-trial chemicals but little or no experi-ence in performing cleanups of agentsof bioterrorism. Outside the militaryand research sectors, little was knownabout the products that are capable ofdestroying key biothreat agents inoffice, warehouse or residential set-tings. A great deal has been learnedabout agents that kill Bacillus anthracisspores and the conditions under whichthey achieve maximum success, butguidelines remain to be developed fordecontaminating bioterrorism agents.As noted in a recent report on cata-strophic bioterrorism, ‘‘Mass deconta-mination is an orphan issue’’.1

INHALATIONAL ANTHRAX: THE BADAND NOT-SO-BAD NEWS

Three forms of anthrax are naturallyoccurring, namely; cutaneous, inhala-tional, and gastrointestinal. Cutaneousand inhalational anthrax are the formsmost likely to result from a bioterror-ism attack using Bacillus anthracis

� Division of Chemical Health

spores. Cutaneous anthrax is charac-terized by distinctive skin lesions andhas a nearly 100 percent cure rate iftreated promptly with antibiotics.Untreated, it has a mortality rate ashigh as 20 percent.2

Inhalational anthrax is a much moredeadly disease. The bad news withinhalational anthrax is that absentboth early detection, when symptomsoften resemble those of influenza, andimmediate aggressive antibiotic treat-ment, the mortality rate is extremelyhigh. Prior to the 2001 attacks, thatrate in the U.S. was estimated to be89 percent.2

Further bad news is that the Bacillusanthracis spore, the form of the bac-terium that causes all three forms ofanthrax, is long lived and very difficultto destroy. Further, the 2001 bioat-tacks demonstrated that sporesreleased inside buildings have thecapacity to re-aerosolize.3 Hence, atsites where persons have developedinhalational anthrax or environmentalsampling results indicate aerosoliza-tion of spores, extensive decontamina-tion processes are needed.

The not-so-bad news about inhala-tional anthrax is twofold. First, person-to-person transmission of the diseasehas not been demonstrated.2 Thismakes the treatment of the disease lessof a threat for health care professionalsonce the victim has been decontami-nated and means that subsequent con-tacts of the victim with family, friends,and co-workers do not put those per-sons at risk of acquiring or transmittingthe disease. Second antibiotics and avaccine are available for exposed per-sons and the cleanup workers who willneed to remediate contaminated facil-ities. Following the 2001 attacks large

and Safety of the American Chemical Society 13Elsevier Inc. All rights reserved.

numbers of postal employees, Con-gressional staff, and staff of a numberof media outlets took prescribedcourses of antibiotics. A number ofthese persons also took the vaccine.

BACKGROUND ON THE 2001ANTHRAX ATTACKS

In the Fall of 2001, several terroristattacks took place in which Bacillusanthracis spores were transmittedthrough the U.S. mail system. In thefirst attack, letters mailed from NewJersey to New York City media outletspassed through the Trenton Processingand Distribution Center (P&DC) inHamilton, N.J., on September 18.The second attack involved a letteror package sent on or after September18 to American Media Incorporated(AMI), a publisher of weekly newspa-pers, in Boca Raton, FL. In the finalattack, letters to Senators Daschle andLeahy entered the Trenton P&DC onOctober 9. The Federal Bureau ofInvestigation subsequently recoveredfour letters: the letter to Tom Brokawof NBC, the letter to the New YorkPost, and the letters to SenatorsDaschle and Leahy. It is believed thatthere were at least seven such letters.4

Twelve cases of cutaneous anthraxand 11 cases of inhalational anthraxresulted from these attacks. Five ofthe persons with inhalational anthraxdied.5,6 Inhalational anthrax cases werereported only after the second and thirdattacks. Nine of the 11 cases were work-ers believed to have been exposed toletters containing Bacillus anthracisspores. The source of exposure in thetwo other cases is unknown.7

Sites at whichworkers developed

inhalational anthraxwere subjected toin-depth cleanupswhich employedfumigation as

the mainremedial tool.

ANTHRAX DECONTAMINATIONS

Numerous sites were contaminatedeither through direct contact withthe source letters or through second-ary (cross) contamination. Amongthese were media offices, postal facil-ities, multiple office buildings onCapitol Hill, and residences. The con-taminated postal facilities includedlarge P&DCs such as the TrentonP&DC, the Morgan P&DC in NewYork City, which processes mail into

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and out of Manhattan, and the Brent-wood facility in Washington, D.C.Numerous smaller U.S. Postal Service(USPS) facilities also experiencedcontamination, as did a number offederal government mail facilitiesdownstream of the Brentwood facil-ity, such as the Department of State(DOS) and the Department of Justice(DOJ) mail facilities.

Two types of cleanups were per-formed in response to the bioterrorismattacks. Environmental sampling de-monstrated that the contamination atmost of the facilities was of a limitedandsurficial nature; such cross-contamina-tion resulted from surface contact withother contaminated items such as let-ters. Surface treatments using liquidagents were used for such sites. Theagents utilized were sodium hypochlor-ite (bleach), aqueous chlorine dioxideand mixtures of hydrogen peroxide andperoxyacetic acid. For each agent, treat-ment conditions were prescribed forefficacy, including concentration andcontact time. For example, EPA deter-mined that a concentration of 500 partsper million (ppm) aqueous chlorinedioxide is effective on hard, non-poroussurfaces after a 30 minutes contacttime.8

Sites at which workers developedinhalational anthrax were subjectedto in-depth cleanups which employedfumigation as the main remedial tool.Fumigations were also performed intwo areas of the Hart Senate OfficeBuilding (HSOB), particularly in Sena-tor Daschle’s suite in which the con-taminated letter to him was opened. Atthis site office staff and the first respon-ders who removed the letter were

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promptly placed on antibiotics, andno one developed inhalationalanthrax. The two air handling unitsservicing the tier of HSOB in whichthe Daschle suite is located were sub-sequently fumigated.

At some sites such as the HSOB, areaswith significant aerosolizable conta-mination were fumigated, other areaswith lesser cross-contamination weretreatedwith liquidagents, and still otherareas in which there was no evidenceof contamination were not treated.

Three chemical agents were used tofumigate sites; namely, paraformalde-hyde (pHCHO), gaseous chlorinedioxide (ClO2), and vaporized hydro-gen peroxide (VHP). Paraformalde-hyde has been routinely used fordecades to decontaminate biosafetyhoods and research and clinicallaboratories.9,10 It was also used tofumigate containment facilities andbuildings utilized in the U.S. biowar-fare program prior to its termination.11

It was also employed to fumigate atleast one textile mill which processedgoat hair12 and a biomedical researchlaboratory facility contaminated withEbola virus.13 Paraformaldehyde hasbeen demonstrated to be an effectivebiocide, killing both vegetative cellsand endospores.9,10 Chlorine dioxideis extensively used in water treatmentand disinfection and in the bleachingof paper. It has many applications inthe food industry. Gaseous ClO2 hasbeen evaluated for use in the biomedi-cal sterilization industry.14 The spori-cidal activity of gaseous ClO2 wasdemonstrated in the 1980s, and thegas was registered for use as a steriliz-ing agent by the EPA in 1988.8 Prior to2001 it had not been used to fumigatebuildings or sections of buildings con-taminated with Bacillus anthracisspores.

VHP is used routinely in the phar-maceutical industry to decontaminatemanufacturing clean rooms and ani-mal toxicology laboratories. It is usedto sterilize containers for asepticallypreserved foods such as fresh milkand fruit juices.15 It has been demon-strated to be an effective sporicide overa range of temperatures and concen-trations.16 Like ClO2, it had not beenused to fumigate civilian facilities orparts thereof prior to 2001.

ical Health & Safety, July/August 2005

Table 1. Technical Issues at Seven Sites with Fumigation Remedies

SiteInhalational

Anthrax CasesNature of

Contamination FumigantVolume

Fumigated (ft3)FumigationApproach

Daschle Suite/HSOB No Aerosolized ClO2a 90,000 All at once

Brentwood P&DC 4 Aerosolized ClO2 >14 million All at onceTrenton P&DC 2 Aerosolized ClO2 �6 million All at onceAMI Building 2 Aerosolized ClO2 670,000 All at onceDOJ mail room No Secondary pHCHOb 8,300 All at onceGSA Building 410 No Secondary VHPc 1.4 million 9 zonesDOS SA-32 1 Aerosolized VHP 1.4 million 10 zonesa Chlorine dioxide gas.b Paraformaldehyde.c Vaporized hydrogen peroxide.

In evaluating the existing fumigantsfor use at a given contaminated site,multiple criteria need to be considered.They include history of usage, physi-cal-chemical properties and acute andchronic toxicity of the agent and anyby-products formed during treatment,and workplace exposure limits. Treat-ment-specific criteria include penetra-tion capability of the agent, methodsfor generation, materials compatibilityboth as to materials that interact withthe fumigant to decrease its effectiveconcentration during fumigation andthose that are adversely affected byexposure to the fumigant, and meth-odologies for removing the fumigantfollowing treatment. Finally, facility-specific criteria such as volume withinfacility to be fumigated, and overalltime for and cost of fumigation needto be considered. Each fumigant hasadvantages and disadvantages; there isno silver bullet. The decision as towhich fumigant to use needs to bemade on a site-specific basis.

Fumigations were performed atseven facilities in response to the2001 anthrax attacks (Table 1); theHSOB, Brentwood P&DC, TrentonP&DC, AMI Building, DOJ postalfacility, General Services Administra-tion (GSA) Building 410, and DOSAnnex-32. Chlorine dioxide was usedfor the first four sites, pHCHO wasused at the DOJ mail facility, andVHP was used to remediate the lasttwo sites. At three sites, fumigation wasperformed of the entire site at one time(Brentwood, Hamilton, AMI), while attwo other sites (GSA Building 410,DOS Annex-32), the entire facilitywas fumigated, but in sub-sectionstreated sequentially. At the other twosites, only a portion of the facility wasfumigated.

Chemical Health & Safety, July/August 200

The volumes fumigated at one timeranged from about 8300 cubic feet (ft3)at the DOJ facility to over 14 million ft3

at the Brentwood P&DC. The Daschlesuite in the HSOB has a volume ofabout 90,000 ft3 on two floors; theremaining four facilities have volumesranging from about 660,000 to 6 mil-lion ft.3,17

The HSOB was the first of thesefacilities returned to productive use;it was re-opened on January 22,2002, slightly more than three monthsafter the contamination occurred. Thecleanup work was conducted on a 24/7 basis; multiple agencies within thefederal government and U.S. militarycontributed to the cleanup, with EPAserving in the lead capacity under anIncident Commander appointed by theCapitol Hill Police Board. The Daschlesuite was fumigated on December 1,2001. Further surface cleanup activ-ities were conducted in that suite; fol-lowing that step all post-remediation(clearance) environmental sampleswere negative for growth of Bacillusanthracis spores. The three-monthtime frame was by far the shortest ofall the cleanups that included fumiga-tions.

Fumigations at three of the other sitestook place in 2002 (DOJ facility, GSABuilding-410, Brentwood P&DC); ano-ther two were fumigated in 2003. Thelast site to be fumigated was the pri-vately-owned AMI Building, whichwas fumigated with ClO2 on July 11,2004. As of October 2004, several of thesites were still undergoing renovationand upgrading activities and had notbeen opened for productive re-use(Table 2).

The remediation time frame at boththe Brentwood and Trenton P&DCswas impacted by the need to wait for

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the contractors to finish cleanup activ-ities with ClO2 at the HSOB. TheUSPS decided to use ClO2 to fumigatethe two P&DCs shortly after that agentwas selected for use in the Daschlesuite, so as to perform cleanups thatwere consistent with that performedon Capitol Hill. The ClO2 generationand scrubbing equipment was movedfrom the Brentwood facility to theTrenton P&DC in April 2003, andthe fumigation at the site occurred inlate October 2003.

At the DOS facility, remedial activ-ities for the entire building did notcommence until after the fumigationof 48,000 diplomatic mail poucheswith paraformaldehyde at the facilitywas completed in June 2002. The AMIBuilding was sold to a real estatedeveloper in Spring 2003, who didnot make a decision on the agent touse and contractor to hire until late2003. The actual cleanup of thisfacility commenced in March 2004with additional environmental sam-pling and removal of items from thefacility and continued until August2004.

Fumigation cleanups have been verycostly. The cost for remediating theDOJ facility of slightly under a halfmillion dollars was by far the leastexpensive. The cleanup of all the siteswithin the Capitol Hill AnthraxResponse cost about $28 million, andthe cost of the remediation of the DOSmail facility was almost $9 million. Thecost for remediating the Trenton andBrentwood P&DCs was about $200million.18

Not included in these costs were thebusiness continuity costs while thefacilities were being remediated andthe charges for renovating the facil-ities, and in certain cases upgrading

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Table 2. Time Frame and Cost Considerations at Seven Sites with Fumigation Remedies

Site

CleanupTime

Framea

(Months)

FumigationTime

Frameb

(Months)

Cost ofRemediation($ millions)

DateReopened Comments

HSOB—Daschle suite/2air handling units

�3 2 28 January 2002 Only site at which remediationperformed on 24/7 basis

Brentwood P&DC 23 9 200 (applies toboth P&DCs)

September 2003 Remediation completedJanuary 2003

Trenton P&DC 28 7 February 2005(exp)c

Remediation completedDecember 2003

AMI Building >37 2 <5 Late 2004 (exp) Remediation completedAugust 2004

DOJ mail room 4.5 0.25 <0.5 March 2002GSA Building 410 32 4.5 ?? Early 2005 (exp) Remediation completed

November 2002, clearedfor re-occupancy June 2004

DOS SA-32 26 3 9 February 2005(exp)

�48,000 diplomatic mailpouches fumigated before remedialprocess begun; fumigations of10 zones took <2 months

a Time frame defined as date from closing of facility due to Bacillus anthracis contamination to date of determining that the site was safe for re-occupancy.b Time frame defined as when equipment for fumigation arrived on-site until completion of fumigation process.c Expected.

them to make them less vulnerable topotential future attacks.

JUDGING EFFICACY OF OVERALLREMEDIATION

The current criterion for judging theeffectiveness of an overall site remedia-tion process is zero growth of Bacillusanthracis spores from all clearanceenvironmental samples. This appliesto all sites, regardless of whether thecontamination occurred through a pri-mary aerosolization event or as theresult of secondary contamination.19

In those instances in which one or moreclearance environmental samples yieldpositive growth of spores, further reme-dial work will generally need to beundertaken. The nature and extent ofsuch additional activities will dependupon the results of the clearance envir-onmental sampling. This criterion doesnot guarantee that all Bacillus anthra-cis spores will have been killed by treat-ment, or that there is zero risk ofdisease, but it does provide confidencethat residual risks of developinganthrax are negligible. It is a publichealth-protective criterion which isbased upon the inability, given the cur-rent state of science, to estimate theminimum number of Bacillus anthracis

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spores necessary to induce inhalationalanthrax in exposed persons.20

The current criterionfor judging theeffectiveness ofan overall site

remediation processis zero growth of

Bacillus anthracisspores fromall clearance

environmentalsamples.

At all seven facilities with fumiga-tions, all clearance environmental sam-ples collected at the conclusion of theremedial activities were negative forgrowth of Bacillus anthracis spores.

LESSONS LEARNED FROM SITESWITH FUMIGATION REMEDIES

As a result of overseeing, and, in onecase conducting, the remediation pro-

Chem

cesses of the sites with fumigationremedies, EPA has learned importantlessons about anthrax cleanups thatwill make future remediations moreefficient, should there be additionalattacks. Keys among these lessonsare the following:

� A

ica

ll contaminated sites have uniquefeatures and should be evaluated onan individual basis.

� F

or sites at which primary aerosoli-zation of Bacillus anthracis sporeshas occurred, fumigation of all or apart of the facility is the defaultremediation process.

� M

ulti-disciplinary teams of expertsshould be assembled by the respon-sible organizations to assess and helpremediate sites contaminated withbiological agents of terrorism. Exper-tise in sterilization science is criticallyneeded to respond to attacks withBacillus anthracis spores. For sitesat which fumigations of very largespaces are planned, chemical engi-neering support should also be soli-cited to evaluate the safety andeffectiveness of the process forremoving the fumigant during andat the end of the treatment (Figure 1).

� I

nput from representatives of therelevant federal, State and local reg-ulatory agencies charged with over-

l Health & Safety, July/August 2005

Figure 1. North Scrubber System for Destruction of Chlorine Dioxide Gas Exiting Brentwood P&DC Facility. Sodium Sulfite andSodium Hydroxide Neutralized Gaseous ClO2 in Scrubber; Residual ClO2 then Removed by Passage of Gas Through ActivatedCarbon Bed Prior to its Exiting Through Stack. A Second Scrubber System (South Scrubber) was Located on the Other Side ofthe Building.

Ch

seeing the cleanup process should beencouraged throughout the entireprocess.

� C

urrently, ClO2 and VHP are theonly practicable fumigants for non-laboratory, civilian sites, given con-cerns about the potential carcinog-enicity of formaldehyde to humans.Further research on the three fumi-gants is needed as to their optimal useparameters, materials compatibilityand costs. All three of the fumigantshave advantages and disadvantages.

� E

nvironmental sampling is key atmultiple stages of the remediationprocess. The advances in samplingapproaches and techniques since2001 need to be incorporated infuture sampling activities. Further,accurate records need to be kept of

emical Health & Safety, July/August 2005

all sampling locations, methods, andresults from each sampling event foruse in judging the effectiveness of theremediation process.

� E

mergency response plans need tobe developed to address worst caseand reasonably expected failure sce-narios during fumigations, andpotential acts of terrorism. Real-timeambient air monitoring is needed,particularly when businesses andresidential areas are in close proxi-mity to the site. Prior to the start ofthe fumigation, two separate con-centrations of fumigant in ambientair need to be established jointlywith the relevant local governmentalauthorities. If the first level isreached or surpassed, the fumigationprocess will be temporarily paused;

if the second level is attained, thefumigation will be terminated.

� L

ong down times occur when fumi-gation is needed to achieve effectiveremediation of the site, especially forlarge facilities. Even under best caseconditions, cleanups currently takemonths to complete.

� T

he costs of remediating Bacillusanthracis contamination are signifi-cant. Business continuity costs andbuilding renovation costs add evenmore to the total cost. At certain sitesjudged especially vulnerable tofuture attack, additional costs willresult from the installation of detec-tion and other equipment to protectworkers and infrastructure.

� D

econtamination waste from reme-diations of contaminated sites pre-

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sents a number of important issues.Each of the three types of waste –disposable personal protectiveequipment, site debris, and deconta-mination water – provides chal-lenges for disposal, particularly asto the facilities that will accept thewaste. The disposal costs are alsosignificant.

The ultimate lesson learned is thatremediation processes for Bacillusanthracis contamination which entailfumigations of an entire facility arecomplex, costly and time-consumingactions.

Another challengewill be assemblingthe right team ofexperts to preparefor and respond

to futureattacks.

RESEARCH NEEDS

The responses to the anthrax attackshave highlighted important researchneeds to enable the country to be moreprepared to address potential futureattacks with a range of biological threatagents. A critical need is the develop-ment of reliable, reproducible, real-timedetection methodologies with extre-mely low false positive and false nega-tive rates notonly forBacillusanthracisspores but also for other key biologicalagents. The USPS is in the process ofinstalling biohazard detection systemsfor detecting anthrax spores in itsP&DCs. These automated systems col-lect a sample over an hour period andthen analyze the samples in the nexthalf hour using polymerase chain reac-tion methodology. In tests to date, thefalse positive rate has been very low.18

The responses to theanthrax attacks havehighlighted important

research needs toenable the countryto be more preparedto address potential

future attackswith a range ofbiological threat

agents.

18

Another need is to develop validatedenvironmental sampling and labora-tory analytical methodologies. Estab-lished limits of detection for Bacillusanthracis spores currently do not exist.Recovery efficiencies of Bacillusanthracis spores from various environ-mental surfaces and media (e.g., non-porous and porous surfaces, air) havenot been well characterized, nor haverecovery efficiencies from the samplesthemselves during the analytical pro-cess. Studies are needed to determinedetection limits for all sample types.

Dedicated testing facilities areneeded in which studies of existingand proposed fumigants can be per-formed to examine a range of propertiesincluding materials compatibility andappropriate contact times for differentconcentrations of specific fumigantssuch as ClO2. Such facilities could alsobe used to demonstrate whether mobiledecontamination systems for variousfumigants are safe and effective. Suchsystems are needed to be prepared torespond to future attacks.

Ultimately, the research should pro-vide data and procedures for returningcritical infrastructure to productive re-use without damage to sensitive equip-ment in as short a time frame as pos-sible.

REAL WORLD CHALLENGES

Given the deaths and economic dislo-cations that ensued from the limitedattacks in 2001, it is important to deter-mine which organizations should havepreparedness plans for biologicalagents of terrorism. Should the orga-nizations be limited to those that areknown targets such as media outlets,governmental office buildings, andpostal facilities? Should organizationswith known vulnerabilities such astransportation centers or sports arenasalso be included? Or should all orga-nizations have preparedness plans, butwith differing levels of complexity?

Further, organizations that developpreparedness plans will need to deter-mine the extent of such plans and thebiological agents covered in theirplans. They will have to decide theextent to which protective actions willbe taken. For example, they will need

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to determine whether to install biolo-gical detection systems and whether toinclude detailed response guidelines aspart of their preparedness plans.

Organizations that should contem-plate developing response plans as partof their preparedness activities arethose for whom an attack on theirinfrastructure would be so cripplingthat preventive action is needed. Fororganizations such as transportationcenters perhaps the financial burdenof such plans could be shared amongmultiple facilities to lessen the burdenon individual organizations. Basedupon the lessons learned from theresponse to the anthrax attacks, tem-plates for responding to future attacksare being prepared by the Departmentof Homeland Security.21

Another challenge will be assemblingthe right team of experts to prepare forand respond to future attacks. One wayto have such teams in place and readilyavailable in case of attacks would be fororganizations with high vulnerabilitiesto establish Technical Advisory Com-mittees that would meet on an annualor biannual basis to provide guidanceto the organization on preparednessand response plans, needed trainingof employees, and regular exercises totest response readiness.Maintenance ofpreparedness in the faceofa longperiodwithout attacks will be a particularlydifficult challenge for many organiza-tions. Technical Advisory Committeesmight be an effective way of dealingwith this challenge.

Most importantly, our nation needsto be prepared for the next bioattack,not just the last one.

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14. Kowalski, J. B. Sterilization of MedicalProducts, Vol. VII; Morrissey, R. F.;Kowalski, J. B., Eds.; Polyscience Pub-lications, Inc.: Champlain, NY, 1998,p. 313.

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16. Joslyn, L. J. Disinfection, Sterilization,and Preservation, 2nd ed.; Block, S. S.,Ed.; Lippincott Williams & Wilkins:Philadelphia, PA, 2001, p. 344.

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