Review of health hazards and prevention measures for response and recovery workers and volunteers after natural disasters, flooding, and water damage: mold and dampness
Environ Health Prev Med
Review of health hazards and prevention measures for response and recovery workers and volunteers after natural disasters, flooding, and water damage: mold and dampness
Eckardt Johanning 0 1 2 3 4 5
Pierre Auger 0 1 2 3 4 5
Philip R. Morey 0 1 2 3 4 5
Chin S. Yang 0 1 2 3 4 5
Ed Olmsted 0 1 2 3 4 5
0 C. S. Yang Prestige EnviroMicrobiology, Inc. , Voorhees, NJ , USA
1 P. R. Morey Environ International Corporation , Gettysburg, PA , USA
2 E. Olmsted Olmsted Environmental Services, Inc. , Garrison, NY , USA
3 E. Johanning (&) Fungal Research Group Foundation (FRG-F), Inc. , 4 Executive Park Drive, Albany, NY 12203 , USA
4 P. Auger Universite ? Laval , Ville de Que ?bec, QC , Canada
5 E. Johanning Columbia University, College of Physicians and Surgeons , New York, NY , USA
Health problems and illnesses encountered by unprotected workers, first-responders, home-owners, and volunteers in recovery and restoration of moldy indoor environments after hurricanes, typhoons, tropical storms, and flooding damage are a growing concern for healthcare providers and disaster medicine throughout the world. Damp building materials, particularly cellulose-containing substrates, are prone to fungal (mold) and bacterial infestation. During remediation and demolition work, the airborne concentrations of such microbes and their byproducts can rise significantly and result in an exposure risk. Symptoms reported by unprotected workers and volunteers may relate to reactions of the airways, skin, mucous membranes, or internal organs. Dampness-related fungi are primarily associated with allergies, respiratory symptoms or diseases such as dermatitis, rhinosinusitis, bronchitis, and asthma, as well as changes of the immunological system.
Microbials; Health; Prevention; Dampness; Mold; Allergens; Toxins; Respiratory health
Also, cognitive, endocrine, or rheumatological changes
have been reported. Based on the consensus among experts
at a recent scientific conference and a literature review, it is
generally recommended to avoid and minimize unnecessary
fungal exposure and use appropriate personal protective
equipment (PPE) in disaster response and recovery work.
Mycologists recommend addressing any moisture or water
intrusion rapidly, since significant mold growth can occur
within 48 h. Systematic source removal, cleaning with
??soap and water,?? and ??bulk removal?? followed by
highefficiency particulate air vacuuming is recommended in
most cases; use of ??biocides?? should be avoided in
occupied areas. Public health agencies recommend use of
adequate respiratory, skin, and eye protection. Workers can be
protected against these diseases by use of dust control
measures and appropriate personal protective equipment. At
a minimum, a facial dust mask such as the National Institute
for Occupational Safety and Health (NIOSH)-approved
N95 respirator should be used for mold remediation jobs.
For any large-scale projects, trained remediation workers
who have medical clearance and use proper personal
protection (PPE) should be employed.
There is growing concern among public and occupational
health experts regarding adverse health reactions and
illnesses encountered in restoration and occupancy of moldy
indoor environments after hurricanes, typhoons, tropical
storms followed by flooding damage, and chronic
dampness. In particular, cleaning and restoration of
waterdamaged and damp homes, businesses, and
mold-contaminated personal items may result in exposure of unprotected
workers, first-responders, home-owners, and volunteers. In
response to the destructive hurricane Sandy (a category 3
hurricane on October 25, 2012 along the northeastern coast
of North America), on March 13?15, 2013 the Fungal
Research Group Foundation, Inc. (FRGF) [a 501(c)3
nonprofit professional?academic organization in the USA that
has held scientific meetings since 1994] gathered an
international group of experts to present state-of-the-art
knowledge and educate restoration and health specialists of
the storm-ravaged areas (http://www.dampnessmold.com).
During this meeting, testimony was heard from volunteers,
workers, and their union representatives regarding
troublesome industry practices, lack of training, and what
would be deemed improper personal protective equipment
(PPE) or unavailability of even simple respiratory
protection (i.e., ??paper masks??). Although some US
governmental agencies now recommend use of a National
Institute for Occupational Safety and Health
(NIOSH)approved ??N95 paper mask?? for respiratory protection,
several occupational health experts expressed their unease
regarding whether this would provide adequate and
sufficient respiratory protection for the complex exposures of
workers in storm- and mold-damaged buildings.
Evidence acquisition and materials
Critical appraisal of a recent specialty conference,
testimony and presentations from an international group of
experts (??Safe and Effective Flood and Mold
Remediation?After the Super Storm Sandy and other Natural
Disasters,?? held at Atlantic City, NJ, March 13?15, 2013 by
the Fungal Research Group Foundation, Inc.; see also:
http://www.dampnessmold.com), and a review of the
relevant literature utilizing search engines such as PubMed.gov
(http://www.sciencedirect.com), and DIMDI (www.dimdi.
de) (search terms: fungi, mold, health, dampness,
remediation, mycotoxin, asthma, hurricane, flood) resulted in the
evidence summary, key findings, and recommendations
Evidence synthesis and results
Exposure sources: fungi and bacteria
Fungi, called ??molds,?? are a heterogeneous group of
organisms including true fungi, lichens, slime molds, and
water molds. Fungi inhabit a wide range of niches and
environments including plants, woods, food, feed, as well
as paper and building materials. Although ordinarily
beneficial in outdoor nature, most ??naturally?? occurring fungi
when growing indoors or on building materials may be
considered ??a danger to health?? of animals or humans
depending on the concentration and exposure route. There
may be from 150 species found indoors to over 600
different species in samples collected from water-damaged
indoor environments. The fungi listed in environmental
samples typically include Penicillium spp., Aspergillus
spp., Cladosporium spp., Rhizopus spp., Paecilomyces spp.,
Aureobasidium spp., Chaetomium spp., Stachybotrys spp.,
and Trichoderma spp. Damp building materials,
particularly cellulose-containing substrates, are prone to fungal
infestation and subsequent mycotoxin production [
With fungal growth and development, their spores are
released into the air, including mycotoxins becoming
]. Production of fungal toxins may also be
influenced by interaction with and the presence of certain
General aspects of fungi and health
Workers may be exposed to fungi or their fragments and
by-products (i.e., allergens, glucans, and mycotoxins) by
inhalation or skin contact and to a lesser degree by
ingestion. In general, the prevalence of skin contact and
dermatitis in workers is as high as 10 %, and unprotected work
is a concern [
]. Inhalation toxicity of mycotoxins appears
to be increased by 20 to 40-fold compared with ingestion
]. Fungi have been associated in case reports, field
investigations, and epidemiological studies with allergy
and respiratory illnesses such as rhinosinusitis and asthma,
but also with irritant or toxic effects, including skin
irritation and other disorders. Mycotoxins are well known in
veterinary medicine and food safety, and regulated in many
countries regarding consumption and food content. These
mycotoxins have also been explored as a possible risk
factor in buildings with mold problems based on
nonallergic clinical presentations of ??sick-building-type??
health complaints [
]. Synergistic inhalation effects of
fungal and bacterial by-products are believed to be
potentially irritating, toxic, teratogenic, carcinogenic, and
]. Although in the ??mold
inspector?? industry, ??toxicity?? is often inferred from the presence
and finding of toxigenic fungi, i.e., Stachybotrys
chartarum, there is no evidence that the detection and
quantification of airborne fungi (by either viable or nonviable
methods) are representative of actual mycotoxin
concentrations. Such tests require highly specialized procedures
and laboratories that are not available to general
investigators (e.g., certified industrial hygienists). Nevertheless, in
studies of molds, endotoxins, and glucans in homes in New
Orleans after Hurricanes Katrina and Rita or the Cedar
River floods, levels of airborne concentrations that had
been associated with adverse health effects were detected
In medicine, fungi are principally known to be a cause
of infections, allergies, and irritant?toxic disorders.
Symptoms reported by patients are often nonspecific and
may relate to reactions of the airways, skin, mucous
membranes, or internal organs. Typical health complaints
and symptoms of patients exposed to allergenic or
toxigenic fungi are listed in Table 1.
Expert reviews of the scientific literature concluded that
dampness-related fungi are highly associated with
allergies, respiratory symptoms, or diseases such as asthma as
well as changes of the immunological system [
There are clinical studies and case reports of adverse health
reactions that include non-allergic adverse effects to the
lungs [sarcoidosis, bleeding in infants; allergic alveolitis
(hypersensitivity pneumonitis)], neurological system
(headaches and cognitive dysfunction), and endocrine and
reproductive organs (thyroid hormonal changes and
menstrual disorders in women), as well as psychiatric
(depression) and rheumatological disorders (joint pain). An
increased risk of cancer from fungal indoor exposure has
been explored, but there seems to be little evidence for this
at this time. Some fungi (maybe in combination with
bacteria) produce chemicals that are known genotoxins and
]. Fungi and their byproducts, such as
1,3-b-D-glucan, mycotoxins, and microbial volatile organic
compounds (MVOCs), have been implicated in these
adverse health reactions and diseases. However, these case
studies are difficult to document and confirm in
epidemiological or experimental studies and have therefore been
considered debatable; further research on these hypotheses
is necessary. Medical conditions associated with fungal and
bacterial exposure during unusual indoor exposure are
listed in Table 2.
Besides encountering large areas of visible mold
conditions in situations such as Hurricanes Sandy, Rita (1997),
Floyd (1999), and Katrina (2005), typically in damp and
wet indoor environments, microbial contaminants are often
at higher levels than they are in the ambient air.
Characteristic health complaints of people living in moldy indoor
environments or workers coming into contact with
excessive fungal exposure are described in the literature as:
burning sensation of the skin or mucous membranes,
irritation and watery eyes, sinus congestion or rhinorrhea, sore
throat and hoarseness, headaches, nausea and vomiting,
severe fatigue and exhaustion, sneezing or cough, chest
tightness, wheezing, chest pain and burning, epistaxis and
hemoptysis, dyspnea, hair loss, and even dizziness,
concentration, and memory problems or feverish/flu-like
]. In most cases, the adverse health
reactions are normally of short duration and reversible,
provided the exposure has been stopped. However, in some
cases the adverse health consequences may be more serious
or may be irreversible . Mold-exposure-related medical
conditions may be diagnosed as atopic dermatitis, urticaria,
rhinitis, sinusitis, bronchitis, asthma, extrinsic allergic
alveolitis (hypersensitivity pneumonitis), organic dust toxic
syndrome (ODTS), and toxic?irritant effects of the skin
and respiratory organ. Although some have proposed
??acceptable threshold levels?? or ??normal limits?? for
indoor mold, variations in sampling strategies and
methodological limitations as well as the different health
outcomes of concern make these very unreliable in practical
settings. Therefore, the consensus among experts is to
generally recommend avoidance or minimizing
unnecessary fungal indoor exposure [
]. In addition,
susceptible populations such as the very young and old,
hospitalized, institutionalized (i.e., prisons), or
immunocompromised people [acquired immunodeficiency
syndrome (AIDS)/human immunodeficiency virus (HIV)], as
well as highly allergic and susceptible individuals will
require special care, protection, and consideration. These
are individuals who should generally not be involved in
water-damage and mold clean-up. During remediation and
demolition work, the airborne concentrations of microbes
and their by-products can rise significantly [
]. In a
recently published study of Hurricane Katrina restoration
workers, 74 % of participants (n = 791) reported
symptoms such as ??transient fever/cough?? (29 %), ??sinus
symptoms?? (48 %), ??pneumonia?? (3.7 %), and
??newonset asthma?? (4.5 %), and a moderate increase in
respiratory dysfunction and toxic pneumonitis was observed
Governmental agencies in the USA such as the New
York City Department of Health, the Occupational Safety
and Health Administration (OSHA), the Federal
Emergency Management Agency (FEMA), the Environmental
Protection Agency, and other public health agencies now
recommend use of a facial dust mask such as the
NIOSHN95 respirator for mold remediation jobs as respiratory
]. However, some have questioned the
adequacy, effectiveness, and protective level of such a
respirator to protect from complex exposure hazards during
remediation work because of a lack of evidence and
supporting data, and have suggested use of an even higher
level of respiratory protection and personal protective
Specific health issues and concerns
Infections caused by fungi are called mycoses and are
categorized as endemic or opportunistic. Opportunistic
fungal pathogens have public and occupational health
importance, especially in subjects with an altered or
weakened immune system, with human immunodeficiency
virus (HIV), or on immunosuppressive medications.
Chronic rhinosinusitis with eosinophilic inflammation of
the airways has been linked to dampness-related fungi from
indoor environments and may be related to the
development of asthma [
Allergy and respiratory diseases
Fungi are a known cause of allergic and respiratory
disease and were identified as one of the major indoor
]. Long duration or intense indoor exposure to
fungi can result in acute hypersensitivity reaction and
chronic diseases. The reported percentages of populations
allergic to molds may vary from 2 to 18 %. A high rate of
asthmatics has been identified in damp buildings and is
reported to be due to allergy to molds [
]. Notably, about
a third of newly diagnosed asthma was attributable to
workplace mold exposure [
]. Workplace-related asthma
occurs in about 25 % of cases and is recognized in about
7 % of patients [
]. Patients can be tested for specific
mold allergy using skin or serological tests to study
immunological responses. However, due to the low
sensitivity of some of the commercially available mold extract
tests, false-negative results are not uncommon.
Additionally, extracts that are generally available for allergy testing
often correspond poorly with the fungi found in indoor
surveys. Patients with an atopy are frequently allergic to
multiple fungal species and manifest type I reactions.
Allergic bronchopulmonary aspergillosis (ABPA) is a
condition where the patient develops an allergy to the
spores of Aspergillus molds [
]. Finally, children are
particular susceptible to development of allergic
complications from exposure to molds and their components [
Hypersensitivity pneumonitis (HP) and organic dust
toxic syndrome (ODTS)
Hypersensitivity pneumonitis (HP), also called extrinsic
allergic alveolitis, is a well-recognized occupational
disease, and fungi are one of the agents causing such
interstitial lung disease. The clinical features, biochemistry,
and pathophysiology of allergic or inflammatory?toxic
reactions to airborne microbial exposure are difficult to
separate. HP can be caused by fungal exposure at work
and indoors [
36, 45, 46
]. Organic dust toxic syndrome
(ODTS), also called toxic pneumonitis, is a nonallergic,
noninfectious form of acute inflammatory lung reaction to
high fungal dust exposure. The differences between HP
and ODTS may be difficult to distinguish. Although
ODTS is believed to be more likely to occur in settings
such as agriculture and recovery facilities, it may also
happen in office and domestic environments during flood
remediation. Immunological blood changes (such as IgG
antibody elevation) can be observed in waste-handling
workers or other occupations with high fungal exposure
Remediation and control
Currently in the USA and many other countries there are no
specific laws or mandates in place that address assessment,
cleaning, and restoration in water-damaged and moldy
public buildings. Based on sentinel case investigations in
the early 1990s in New York City [
], guidelines now
exist for the assessment and remediation of primarily
??visible?? mold indoors  based on an expert consensus
document, which has now been widely adopted. However,
much of what has become ??industry standard?? in the
restoration industry is largely a combination based on
professional experience, cost considerations, expert opinions,
and practical necessities. In addition to visible mold, also,
??hidden?? mold and residual biomass should be
investigated and removed. For certain populations, such as the
very young and old, immunodeficient or impaired
individuals or highly sensitized people, special precautions and
clean-up procedures should be considered, since they are
likely to be more susceptible and at higher risk for adverse
health reactions. Many different remediation approaches
have been applied with more or less success, but often also
expose unprotected workers and building occupants to
preventable harmful situations. In many cases, the
questionable indoor use of a ??biocide?? is promoted by
practitioners and commercial suppliers with insufficient evidence
for its effectiveness and safety. This may contribute to
workers? exposure to agents such as hydrogen peroxide,
isopropyl alcohol, bleach, quaternary amines, or other
proprietary products. However, hygiene experts have
questioned the benefit and use of such products for health
]. Though fully completed remediation may
result in improved fungal air counts, failure of air quality
improvement may still be noted because residual
non-viable and possibly toxic fungal by-products have not been
]. Mycologists recommend addressing any
moisture or water intrusion immediately, since significant
mold growth can occur within 48 h. Efforts to dry affected
areas should be started as soon as possible. Systematic
source removal, cleaning with ??soap and water,?? and ??bulk
removal?? followed by high-efficiency particulate air
(HEPA) vacuuming is generally recommended in most
cases. Workers can be protected against these microbial
exposures and related diseases by use of dust control
measures and appropriate personal protective equipment.
For any larger-scale projects [defined by the New York
City Department of Health (NYCDOH) guideline as
??greater than 100 square feet in a contiguous area??] trained
remediation workers should be medically cleared and use
personal protective equipment (PPE) such as proper
respiratory, skin, and eye protection. However, increased
respiratory protection levels require medical clearance,
respirator certification, and training, which contribute to
additional costs and project management for contractors
and employers. Mold remediation procedures for North
American and Western European buildings have been
summarized in recent publications [
references are available online for guidance [54, 55, http://
(http://iicrc.org/standards/iicrc-s500/), and DHHS
(NIOSH) publication number 2013-102]; however, industry
compliance and documented effectiveness are mostly
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