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 by-products 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. 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 high-efficiency 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.
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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 water-damaged 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.ncbi.nlm.nih.gov/pubmed), ScienceDirect (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 presented below.
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 [1–3]. With fungal growth and development, their spores are released into the air, including mycotoxins becoming airborne [4–6]. Production of fungal toxins may also be influenced by interaction with and the presence of certain bacteria [7, 8].
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 [10, 11]. 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 non-allergic clinical presentations of “sick-building-type” health complaints [12, 13]. Synergistic inhalation effects of fungal and bacterial by-products are believed to be potentially irritating, toxic, teratogenic, carcinogenic, and immunosuppressive . 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 [15, 16].
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 [14, 17–19]. 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 carcinogens [20–27]. Fungi and their byproducts, such as 1,3-β-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 reactions [14, 28]. 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 [30–32]. 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 [33, 34]. 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 “new-onset 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 NIOSH-N95 respirator for mold remediation jobs as respiratory protection . 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 equipment (PPE).
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 [37–39].
Allergy and respiratory diseases
Fungi are a known cause of allergic and respiratory disease and were identified as one of the major indoor allergens . 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 [4, 48], 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 reasons . 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 addressed . 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 [52, 53]. Several references are available online for guidance [54, 55, http://www.epa.gov/iedmold1/cleanupguidelines.html, IICRC (http://iicrc.org/standards/iicrc-s500/), and DHHS (NIOSH) publication number 2013-102]; however, industry compliance and documented effectiveness are mostly unknown.
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Johanning, E., Auger, P., Morey, P.R. et al. 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 19, 93–99 (2014). https://doi.org/10.1007/s12199-013-0368-0