Indoor Air Quality:
Mold in the schools
By Chris Randolph, M.D.
Associate Clinical Professor
Yale Affiliated Hospitals
Waterbury, CT
Learning objectives: Outlines
To familiarize the healthcare
provider with:
1.
Mold associated illness in
schools:
a.
b.
c.
2.
The Role of fungi in the
Environment.
The health impact on schools.
The role of toxigenic fungi.
Diagnosis and remediation
of mold in the school.
Definitions
o
o
o
Fungus Gr sponge: ”Any of a large division of
thallophytes including molds, mildew,
mushrooms, rusts and smuts, which are
parasites on living organisms or feed upon dead
organic matter”
Reproduce by spores and lack chlorophyll, true
roots, stems or leaves. (Webster’s New World
Dictionary 3rd college edition 1994 MacMillan
p546-7)
Mold is “downy or furry growth on the surface
of organic matter caused by fungi especially in
presence of dampness or decay.” (Webster’s
New World Dictionary 1994p873)
Definitions
o
Fungal Related Chemicals:
o
o
o
o
Metabolites: Toxins
Components or byproducts (VOC): Ergosterol, B(1-3)
glucan, VOC (volatile organic compounds)
Mycotoxin: nonvolatile secondary metabolite of
filamentous fungi that is toxic to vertebrates
Produced by many fungal spores and many toxins by
same species i.e. Penicillium, Alternaria, Aspergillus,
Fusarium as well as Stachybotrys. (Webster’s 1994/
Google) (Muilenberg M Current Views All/Imm 2004)
CASES: Mold Associated Illness
in Water Damaged Schools
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12 y/o w/f developed new
onset “asthma” in a school
adjacent to a waterfall.
Middle school children
developed nonspecific
rash, cough and/or
influenza- like symptoms in
a newly constructed school.
High School guidance
counselors developed
influenza - like symptoms
Remediation with decline in
symptoms
Introduction: Ecology
Mold represents a generally
benign saprophyte
Manufacture of antimicrobials to
cheese
Now health concern stifling home
sales, increasing insurance,
affecting schools and taxpayers as
well with poorly documented
health problems
Texas insurance companies /Ed
McMahon/Michael Jordan/School
closures/State Farm and others
eliminate coverage/millions in suits
for attorneys (“Mold is gold”).
ChapmanJA et al:Toxic mold:phantom riskvs science.Ann. Allergy2003:91;222-32
Belkin L.Haunted by mold.NYTimes Magazine8/12/2001p28
Ecology (Chapman 2003)
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Present 559 million years ago or
earlier in peaceful coexistence
Absorb water from soil, wood,
decaying organic matter
Size microscopic to some of
large, multi cellular organisms
(6.5km2 in Washington State(3
counties): Armillaria ostoyae
fungus)
Include 1.5 million species /
100,000 identified / 10 primary
pathogens remainder saprobic
Include toadstools, mildews,
puffballs, yeasts, smut, rusts
occupy 25% of earth biomass
Perfect and imperfect classes
Chapman JA,et al.Toxic mold:phantom risk
Vs science.Annals Allergy,Asthma,Imm.
2003;91:222-232
Ecology (Chapman 2003)
Common indoor CommonOutdoor:
Cladiosporium
Penicillium
Aspergillus
Alternaria
Aureobasidium
Basidiospores
Cladiosporium
Ascospores
Alternaria
Penicillium
Aspergillus
These require continuous O2,
water, organic material and
suitable temperature for growth.
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ChapmanJA et al AnnAll.2003;91:222-32
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(HealthySchools Network,,Albany,NY.
www.healthyschools.org

Acremonium: produces toxin
Alternaria: carpets, textiles,
window frames in building
interiors
Aspergillus flavus water
damaged carpets,
Aspversicolor damp wood or
wall paper glue
Cladosp. in supply ducts
Stachybotrys greenish black
grows on cellulose
Penicillium produce
mycotoxins (Pexpansum,
Pchrysogenum)
Fusarium in humdifiers
Trichoderma in paper source
of antibiotics toxic to
humans
Fungi: growth conditions
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Atmospheric conditions :
Require 70-90% relative humidity
Grow optimally at 20-40o C
Wide variety host requirements
Some grow in hot, dry climate
(xerophilic)
(Terr A.The role of mold in disease.
AmAcadAllAsthmaImm meeting: San
Francisco,California 3/04)
Fungi: Habitat
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
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
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Outdoors: Ubiquitous: airborne globally except
polar caps
Indoors
30-70% of outdoors
From outdoor penetration
Or indoor source i.e. plant or garbage
Primary host: plant especially crops
Saprophytic colonization or pathogenic (invade
tissue) (Terr A. The role of mold in disease
(and non-disease. AAAAI 3/04)
IMPACT OF FUNGI ON
HEALTH ?
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Agent
Source
Pathway
Adequate dose
Outcome
Null hypothesis: Damp, cold and moldy
environments are not associated with
poorer health.
Fungi
o
o
o
o
Areas of medical concern
Allergens
Infectivity
Toxins
Terr A.The role of mold in disease and nondisease.AmAcadAllAsthma
Imm. Meeting. SanFrancisco ,California ,3/04.
Toxic mold:
phantom risk vs science
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Mold associated disease :need for
controls and standards for exposure
Length exposure and individual
sensitivity
4 categories:
Anecdotal evidence
Case studies
Epidemiologic studies
Experimental evidence
Consequences of low level mold unknown
Synergism with indoor aerosols
Mold panic replace with science
Burge,Annals 2003;91:217-219
Chapman et al Annals All2003;91:222-232
Dales RE,CakmakS,BurnettRT,et al.Am J RespCrit Care Med 2000;162(6):2087-90.
Indoor Air Quality in Schools
(Dishop,2002)
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Airtight schools :1960-1970”modular format “was walled in w/o installation of
adequate air circulation. (Morris,AB. Does design make a difference? Conf
AIAComm Arch.Educ.AIA 1997)
Poor maintenance leads to water injury medium for mold and fungal allergen
Sources indoor air quality: covered air supply, return ventilation, improperly
maintained radiator and air filters, ins. sealed cleaning and maintenance
chemicals. Wooden construction >concrete (Meklin T.AIHA
Journal2003;64:108-116)
Other sources classroom pets, second hand smoke,
labs, copier, furnace room vents and ventilation
system, water and moisture injury, eating facilities,
upholstered furniture.
Children most vulnerable particularly with allergic
rhinitis and asthma per Institute of medicine
because they are low to ground have less body
mass and breath more rapidly.
AAP Statement: Damp mold ridden environment
is unhealthy particularly for individuals with
respiratory conditions.
Dishop ML. Maintaining Environmental Cleanliness in School. Suppl JSchNursing 2002 (Oct):23-26
DishopML.Maintaining environmental cleanliness in school.SupplJSch Nurs
October 2002.
Total airborne and viable
fungi in schools
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Total airborne (Daisey et al Indoor Air 2003) and
surface fungi in 13 classrooms in 6 Florida schools in
10 papers.
Health complaints: stuffy sinuses, sore throat,
respiratory illness, lethargy, itchy eyes and runny
nose. Concentration >1000CFU/m3 in one complaint
and non-complaint all others <700CFU/m3 (Bates and
Maffy,1996)
Average and maximum total viable molds measured in
96 classrooms in 38 Swedish schools: 500CFU/M3
and 4,500CFU/m3 (Smedje et al, 1996, 1997)
Carpeted 1900CFU/g dust vs. bare floors
950CFU/g(p=.0.002)
Most prevalent genera: Penicillium, Fusarium,
Alternaria and Cladosporium (Gravesen et al,1986)
Reference
History
Phy. Exam
Affected
Bldg.
Spec. mold(s)
implicated
Croft et al 1985
5 persons: cold, flu, sore throats,
diarrhea, headaches, fatigue, dermatitis,
alopecia, malaise
Repeatedly
Neg.
Home
Stachybotrys
species
Brunekreef et al
1989 22
6273 US children (respiratory
questionnaire) no control subjects
Not done
Homes
Total molds,
spores
Platt et al
1989 25
1169 UK children in 597 households:
excess bad nerves, aching joints, nausea
and vomiting, backache, blocked nose,
fainting spells, constipation,
breathlessness
Not done
Homes
measured
Dampness or
mold
Total molds,
spores
Strachan et al
1990 24
Children with asthma wheezed more in
homes with higher mold counts
Yes,
Spirometry
Homes mold
quantitation
Total molds,
spores
Li & Hsu
1996 23
1370 Children : questionnaire for selfreport of dampness, mold & respiratory
symptoms
Not done
Homes
Total molds,
spores
Cooley et al
1998 20
622 Adult workers at 48 schools with
indoor air quality complaints: no control
subjects
Not done
Schools
Penicillium
species,
strachybotrys
species
Johanning et al,
1999 21
Descriptive study: 22 children and 125
adults with multiple symptoms
Done, not
reported
Homes (no
data on fungal
exposure
strachybotrys
species
Santilli &
Rockwell
2003 27
Rhinitis questionnaire: 85 students &
teachers
Not done
2 schools
Total molds,
spores
16
TerrA.JAll Clin Imm2004;113:221
Cooley J.Occupational Environ Med 1998:55:579-584
Mold in Schools: Studies
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Allergy in form of RAST to molds and (+) PST particularly Aspergillus
associated with IgG antibodies to molds found in mold damaged building.
No association was found IgG to mold and exposure in
school.(TaskinenTMetal.Allergy:2002.57(1)9-16)
Sinusitis in teachers associated with elevated mold specific IgG to multiple fungi
including Aspergillus and Stachybotrys with decrease in IgG on 2 year followup with
sinusitis/bronchitis.(PatovirtaetalIJOMEH2003;16(3)
Association between elevated IgG to Penicillium notatum and E.amstelodami and
moisture damage in school.(HyvarinenA .ArchEnHlth2003;58(5):275-83)
Mold in floor dust had no positive association with building related symptom.but 5/8
symptoms secondary to asthma ,hayfever,recent airway infection or psychosocial
factors.(Meyers:IndoorAir2004;14:65-72)
Childrens’ perception of symptoms increased after publicized that exposure to mold in
schools related to cough,wheezing and joint pains.(Handal Get al Indoor Air
2004;14:87-91 )
Mold in schools
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33% U.S. public schools need
extensive repair(6/96GAO)
Two Connecticut public
schools (Fairfield County)
tested using multiple air
quality testing methods with
standard for healthy indoor
environment for total mold
spore counts 1,000spores/m3
In both schools counts were
elevated (1st : 6000-50,000
sp/m3, 2nd 2-9000 sp/m3)
with associated allergic
symptoms. Both were
remediated. The first school
was demolished and rebuilt.
Santilli et al :Ann Allergy Asthma Imm.2003;90:203-208
Santilli J et al. Fungal contamination of elementary schools: a new
environmental hazard.Ann Allergy Asthma Imm2003;90:203-8.
Santilli J etal.Fungal contamination of elementary schools:a new environmental hazard
.Ann Allergy Asthma Immunol 2003;90:203-8
Fungi: Environmental assessment
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Air sampling: examples Standard > 1000sp/
m3, 100 cfu/m3, 75% (I-O).
1. Viable: culture plates colony counts
2. Nonviable: spores (spores/m3)
3. Surface sample (swipe) Qualitative only
Multiple samples: agitation/indoor /outdoor
Good labs certified
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

www.aiha.org,
www.aaaai.org,.
www.paaa.org
Terr A. The role of mold in disease and non disease, Amer, Acad All Asthma Imm
Meeting San Francisco, California 3/04
Table 1 Turner Environmental’s Testing of Mckinley Elementary School Revealed
Severe Mold Contamination of the Wall Cavities and Rugs
Carpet Samplings
Colony Forming Units/Gm
Room 117
108,500,000
Room 118
20,120,000
Room 221
1,970,000
Wall Cavity Samplings
Mold Spores/m3
Room 107
156,666
Room 117
106,667
Room 121
120,000
Fungal Contamination of Elementary schools: a new environmental hazard,
Santilli J, Rockwell W; Ann Allergy Asthma Immunol 2003;90:203-208
Colony Forming
Units/m3
Figure 4 Results of ASHA testing indoor air quality at Mckinley Elementary School
1400
1200
1000
800
600
400
200
0
1297
908
872
567
531
425
412
Faculty
Room
Room 220 Caferteria Room 221 Room 218 Room 210 Room 222
264
260
Media
Room
Outdoors
Room
Fig 5 Results of Turner Environmental testing indoor air quality at Mckinley Elementary School
Total Mold Spores
Counts/m3
60,000
53,000
50,000
40,000
30,000
20,000
6,500
10,000
1,900
0
Room 107
Gym
Outdoors
Room
Fungal Contamination of Elementary schools: a new environmental hazard, Santilli J, Rockwell W; Ann Allergy Asthma
Immunol 2003;90:203-208
Fungal Contamination of Elementary schools: a new environmental hazard, Santilli J, Rockwell W; Ann Allergy Asthma
Immunol 2003;90:203-208
vomiting
Fatigue
Runny Nose
Coughing
Headaches
Symptoms
Flu
symptoms
Congestion
Irritated
eyes
New or
aggravated
Asthma
Some less common symptoms:
fever, vomiting, nausea, nosebleeds, dizziness, memory loss, diarrhea and
changes in behavior Mycotoxin related symptoms
MuilenbergML.Toxigenic fungi.Current Views in All Imm V;XXXII I/04. MedCollGeo.
Amr S et al.Environmental Allergens and Asthma in Urban Elementary Schools. Ann Allergy Asthma Immunol 2003;90:34-40
Mold in schools
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Skin prick test findings from moisture and mold damaged
schools: Mold allergy in a 3 year follow up disappeared in 2
children and developed in 5.
5/6 of children with reactions >/= 3mm to molds had (+)
response to other allergens
5 children had clinical atopy/2 asthma
All six children had been exposed to moisture and dampness in
the school buildings
Most reactions to molds in child >14y with multiple SPT
reactions to common allergens but no association with asthma
Immonen Jet al Pediatric Allergy and Imm.:2001;12(2):87-94
Toxigenic Fungi
M.L. Muilenberg
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Livestock exposures to mycotoxins
Human food and mycotoxins
The toxigenic fungi and their mycotoxins
 Alternaria, Aspergillus, Fusarium, Penicillium,
Stachybotrys
Respiratory exposures to mycotoxins
Sampling and exposure
Recommendations
Summary
Muilenberg M.Toxigenicfungi .Current Views in Allergy Immunology.2004;
VolumeXXXII.Program4(January)Medical College of Georgia.
Mycotoxins (Etzel RA,JAMA 2002)
Aflatoxins
Aspergillus Flavus
Corn
GI/ Neuro
Clavine alkaloids
Claviceps Fusiformis
Millet
GI/ Drow.
Ergometrine
C. Purpurea (St. A Fire) Barley
GI/ N/
Gang
Fumonisms
Fusarium (horse, swine) Corn
N/P/Death
Cyclopiazonic
Aspergillus
Millet
GI/ Giddy
Ochratoxin
Penicillum / Asp
Grains
Renal
T 2 Toxin
Fusarium (cattle)
Corn
Abortion
Trichothecenes
Fusarium / Asp
Wheat
GI
Tremorgens
Asp/ Pen/ Muc/ Rh/
Cep
Grass/
Alf
GI/ N
Slaframine
Rhizo (horse, cattle,
sheep)
Gr/ Wh
GI/ N
Etzel RA.Mycotoxins.JnlAmer.Med Ass.2002;287(4):425-7.
Human Stachybotryotoxicosis
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By ingestion: 1930’s in Siberia horses fed moldy grain
developed agranulocytosis, GI hemorrhage and ulceration
similar reports in sheep, other animals and farmers.
1942 USSR Academy of Sciences (VG Drobotko)
By inhalation never proven in humans would require
massive doses seen in agricultural or remediation
settings (x10 to 6th power or more spores/mm3)
2.1 x 106 spores / m3 for infant 15.3 x 106spores /m3
for an adult.
Acute interstitial pulmonary hemosiderosis (AIPH)
(Terr A. Mold in disease and non-disease AAAAI3/2004)(Muilenberg M
Current Views Allergy Immunology 2004; Volume XXXII. Prog4. Med.
CollGeo.
Summary continued
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CDC investigation 1999

Conclusion:
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Human diseases from mold:

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A possible association between acute pulmonary
hemorrhage…and (mold) exposure …was not proven
(CDC.Report of working group on pulm. hemorrhage and
hemosiderosis, CDC and Prevention,1999)
Specific molds produce infectious or allergic disease
Toxic conditions from inhalation of mold spores is
unproven. (Terr AThe role of mold in disease and nondisease. AAAAI 3/04)
Current scientific evidence does not support…that
human health has been adversely affected by inhaled
mycotoxins in home, school or office environments.
ACOEM JOEM 2003;45(5):470-78
DIAGNOSIS
&
REMEDIATION
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NHLBI:
Goals for Healthy School
Environment
Keep temperature and humidity
appropriate
Maintain HVAC systems
Dry up damp and wet areas within
1-2 days
Minimize exposure to triggers:
smoke, chemical vapors, chalk dust,
mold, fumes and animals.
Approach for Patient
o
o
o
o
Log of walk through school :
check for mold or water
damage, stagnant water,
inadequate ventilation, air
intake grills
Check ceilings, tiles, walls
looking for water stains
including inside closets,
boxes and behind furniture
Damp musty smell or visible
colored deposits green,
brown, yellow or black should
be taken care of immediately
to prevent spreading
Tell your doctor
(Healthy Schools Network, Inc:Albany,NY www.healthyschools.org)
Evaluation of Building related
illness by specialist
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Comprehensive history: nature of symptoms, home, work
environment, medical and family history.
Physical exam: signs of systemic fungal, Tb and pneumocystis
pneumonia
Atopy: skin and serologic testing and PFT pre and post
bronchodilator
Chest x-ray /CT of chest
Supportive testing serologic Ig to fungi, for humoral and cell med
immunity and pneumonitis
Environmental assess: walk through and sample measurement of
vacuumed dust sample and water damaged areas by prof. hygienist
Measurement of total symptom scores inside and outside
Pre-bronchodilator and post-bronchodilator measurement of
spirometry inside and outside home or workplace every 2-4 hrs
while awake and correlate with environmental exposure
measurement.
Tools for schools EPA (Environmental Protection Agency)
OSHA (Occupational Safety and Health Administration)
Chapman et al Annals Allergy,Asthma,Immunol2003;91:222-232
TABLE : METHODS FOR IDENTIFICATION OF INDOOR FUNGAL EXPOSURE
Method
Advantage
Disadvantage
Implications
Visual id air sample
Rapid for airborne
exposure sensitive
No species,laborious
Inhaled species
associate disease
Culture
Identify species assay
for mycotoxins
Laborious must grow Inhaled spores cause
on media not
disease
sensitive
Questionaire
Inexpensive
Not specific or
validated
Allergen Immunoassay
Very sensitive specific
for genera
Monoclonal too
specific
Measures allergic
potential
Mycotoxins
Toxic potental of
exposure
Assay difficult to
reproduce: EIA
Chromotography
Organ toxicity
Ergosterol
Fungal Mass
Not useful for taxa
None
EPSs
To identify genera
B(1-3) glucan
Fungal Mass
Non-fungal sources
affect
Inflammation
VOCs(Volatile organic
compounds)
PCR need standards
Specific for taxa
Non-fungal sources
affect
Irritant
None
BUSH R,PORTNOY J.The role and abatement of fungal allergens in allergic disease.JALLERGY CLIN
IMMUNOL2001;107:S430-440
Results Report
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Scope of work
Site physical description
Review of mechanical systems: HVAC, etc
Sample location and circumstances
Summary analytic results and recommendations
including walk-through
Analytic reports: IAQ measurements with spore counts
by genus indoor and outdoor ratio, rooms sampled,
bulk and surface samples , vacuum dust samples in
CFU/gm or m2,instruments used, lab reports (Portnoy
J Allergy Clin Imm.2004;113(2):190-198
Assessment and remediation of
indoor fungi
Prompt remediation of contaminated material and infrastructure repair.
Prevent contamination through proper building, heating, ventilation, air
conditioning (HVAC) maintenance and repair of water damage. (Tools)
More research needed to link health outcomes and mycotoxins.
Env assessment: visual inspection HVAC, ceilings, gypsum wallboard,
paper and cellulose containing surfaces.
Indoor and outdoor comparisons (no standard or human dose response)
range upward from 100CFU/m3.School closures and rebuilding.
Remediation of water damage or condensation immediately (RH<60%)
control mold by 4 different levels 10 sq ft to 100sq ft and HVAC (NYC
Dept Hlth) (USEPA, OSHA, Amer Conf Gov Ind. Hygenists) see WWW
Concern little science to support public reaction (“black box”).
Chapman et al .Toxic mold:phantom risk vs science.Annals Allergy Asthma ,Immunol 91:222-232
Checklist for mold remediation
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Communicate with building occupants at
all times with designated person
Plan remediation: trained remediation
personnel, proper containment
equipment and personal protective
equipment, cleanup mold items and
drying non-moldy materials within 48
hours.
Remediation moisture and mold
problems:
Fix moisture problems including
maintenance and/or repair
Eliminate porous material infested with
mold that can’t be cleaned.
EPA.Mold remediation in schools and commercial buildings .EPA402-K-01-001.3/01.
Conclusions



Rigorous prospective studies linking exposure to
mold in water damaged school environments and
subsequent human disease need to be done.
In the interim if after careful inspection more
extensive water damage (>10 sq ft) is suggested
especially with symptomatic personnel, then
professional investigation by OSHA and industrial
hygienist with micro and bulk sampling as well as
appropriate air sampling indoor and outdoor is
recommended.
Remediation to correct existing and prevent
further water damage should then be done by
professionals.
Resource list: EPA

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
IAQ (Indoor air quality) in schools
www.epa.gov/iaq/schools/index.html
Mold remediation in schools
www.epa.gov/iaq/pubs/molds.html
Indoor air quality(IAQ)home page
www.epa.gov/iaq
EPA IAQ Clearinghouse
iaqinfo@aol.com
Mold Remediation Labs
Aerobiology Instruction &
Research
465 Washington St., #1
Brookline, MA 02446
Aerobiology Lab Assoc., Inc.
11800 Sunrise Valley Dr, Suite
1250
Reston, VA 20191
Environmental Microbiology Lab
10636 Scripps Summit Ct., Ste. 103
San Diego, CA 92131
P&K/Aerotech Microbiology
Services, Inc.
1936 Olney Ave.
Cherry Hill, NJ 08003
(RT-PCR; culture, spore ID)
Environmental Testing and
Technology, Inc.
4176 Mt. Hukee Ave.
San Diego, CA 92117
Air Quality Sciences, Inc.
Atlanta, GA
(770)933-0638
EMSL Analytical, Inc.
N. Miami Beach, FL
(800)220-3675
References
1.
2.
3.
4.
Dales RE, Cakmak S, Burnett RT et al. Influence of
ambient fungal spores on emergency visits for asthma
to a regional children’s hospital. Am J Respir Crit
Care Med.2000;162(6):2087-90
Platts-Mills TAE Solomon W. Aerobiology and inhalant
allergens. Chapter 19.Allergy:PrinciplesandPractice.ed
E Middleton, CE Reed, EF Ellis, NFAtkinson et al.
Fourth edition Volume 1 :Mosby St
Louis,Missouri,1993:469-528
Belkin L. Haunted by mold. NY Times Magazine
August 12, 2001 Late ed. Section
6,Column1,p28(16pages)
Webster’s New World Dictionary .Copyright
1994,Simon and Schuster ,Macmillan New York, New
York p873.
References
5. Biology 5 thed NACampbell, JB Reece , LG
Mitchell. Chapter 31.Fungi. P 574-588.
Addison Wesley Longman, Inc 1999 Menlo
Park ,California
6. Terr A. Role of mold in disease and
nondisease. AAAAI meeting SanFranciso
3/04.
7. Chapman JA,TerrAI, Jacobs et al. Toxic
mold: phantom risk vs science. Annals
Allergy 2003;91:222-232
References
8. Burge HA Fungi: Toxi killers or unavoidable
nuisance. Annals Allergy, Asthma, Immunol
2001:87(Suppl) 52-56.
9. Burge HA. Bioaerosols and the scientific
method. Ann Allergy Asthma Immunol
2003:91:217-219
10. Healthy Schools Network. Albany, NY
www.healthyschools.org
11. Bush RK ,Prochnau JJ. Alternaria-induced
asthma. J Allergy Clin Immunol
2004;113:227-34.
References continued
12. Dishop ML. Maintaining environmental cleanliness in
school. Supplement in the Jnl School Nursing
.2002(October):23-26
13. Morris,AB.Ed.(1997).Does design make a difference:
A conference of the AIA Committee on Architecture
for Education. Scottsdale:American Institute of
Architects.
14. Meklin T, Hyvarinen A, Toivola M, etal. Effect of
building frame and moisture damage on
microbiological indoor air quality in school buildings.
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