Mary Brandt, PhD,1 Clive Brown, MBBS,2 Joe Burkhart, MS,3 Nancy Burton, MPH,3 Jean Cox-Ganser, PhD,3 Scott Damon, MAIA,2 Henry Falk, MD,4 Scott Fridkin, MD,1 Paul Garbe, DVM,2 Mike McGeehin, PhD,2 Juliette Morgan, MD,1 Elena Page MD,3 Carol Rao, ScD,1,5 Stephen Redd, MD,2 Tom Sinks, PhD,2 Douglas Trout, MD,3 Kenneth Wallingford, MS,3 David Warnock, PhD,1 David Weissman, MD3
1National Center for Infectious Diseases
2National Center for Environmental Health
3National Institute for Occupational Safety and Health
4Coordinating Center for Environmental Health and Injury Prevention
5Office of Workforce and Career Development
The material in this report originated in the National Center for Environmental Health, Agency for Toxic Substances Disease Registry, Howard Franklin, MD, Director, and the Division of Environmental Hazards and Health Effects, Michael A. McGeehin, PhD, Director.
Corresponding preparer:Clive Brown, MBBS, National Center for Environmental Health, CDC, Century Center, Building 2400, MS E-39, Atlanta, GA 30329. Telephone: 404-498-1000; Fax: 404-498-1088; E-mail: email@example.com.
Extensive water damage after major hurricanes and floods increases the likelihood of mold contamination in buildings. This report provides information on how to limit exposure to mold and how to identify and prevent mold-related health effects. Where uncertainties in scientific knowledge exist, practical applications designed to be protective of a person's health are presented. Evidence is included about assessing exposure, clean-up and prevention, personal protective equipment, health effects, and public health strategies and recommendations. The recommendations assume that, in the aftermath of major hurricanes or floods, buildings wet for >48 hours will generally support visible and extensive mold growth and should be remediated, and excessive exposure to mold-contaminated materials can cause adverse health effects in susceptible persons regardless of the type of mold or the extent of contamination.
For the majority of persons, undisturbed mold is not a substantial health hazard. Mold is a greater hazard for persons with conditions such as impaired host defenses or mold allergies. To prevent exposure that could result in adverse health effects from disturbed mold, persons should 1) avoid areas where mold contamination is obvious; 2) use environmental controls; 3) use personal protective equipment; and 4) keep hands, skin, and clothing clean and free from mold-contaminated dust.
Clinical evaluation of suspected mold-related illness should follow conventional clinical guidelines. In addition, in the aftermath of extensive flooding, health-care providers should be watchful for unusual mold-related diseases. The development of a public health surveillance strategy among persons repopulating areas after extensive flooding is recommended to assess potential health effects and the effectiveness of prevention efforts. Such a surveillance program will help CDC and state and local public health officials refine the guidelines for exposure avoidance, personal protection, and clean-up and assist health departments to identify unrecognized hazards.
On August 29 and September 24, 2005, hurricanes Katrina and Rita, respectively, made landfall along the Gulf Coast. After both storms, levees were breached, leading to massive flooding in New Orleans and surrounding parishes.
The duration of flooding, the extent of flooding, and the number of structures flooded in New Orleans as a result of hurricanes Katrina and Rita in August and September 2005 made the likelihood of massive mold contamination a certainty. Many structures remained flooded for weeks after the hurricane and became saturated with water. An assessment of homes in New Orleans (Orleans Parish) and the surrounding parishes of St. Bernard, East Jefferson, and West Jefferson (excluding the 9th Ward) identified an estimated 46% (>100,000 homes) with some mold contamination; approximately 17% (40,000 homes) had heavy mold contamination (1).
Recent parallels to the kind of flooding observed in New Orleans as a result of hurricanes Katrina and Rita occurred in 1997 in Grand Forks, North Dakota, and in 1999 in North Carolina after Hurricane Floyd (2). The number of structures affected was much smaller in North Dakota than in New Orleans, and the population affected in North Carolina was much more dispersed than the population affected in New Orleans. In North Carolina, a reported increase in persons presenting with asthma symptoms was postulated to be caused by exposure to mold (2). In 2001, flooding and subsequent mold growth on the Turtle Mountain reservation in Belcourt, North Dakota was associated with self-reports of rhinitis, rash, headaches, and asthma exacerbation (3).
This document was initially prepared by CDC as a guide for public health officials and the general public in response to the massive flooding and the anticipated mold contamination of homes and other structures along the U.S. Gulf Coast associated with hurricanes Katrina and Rita (4). A workgroup was convened of CDC staff with expertise in relevant subject areas. This included medical epidemiologists, environmental epidemiologists and occupational epidemiologists, industrial hygienists, infectious disease physicians and mycologists. The framework for the document was decided by consensus discussions, and workgroup members were assigned to research and to write different sections. The members produced individual written summaries, which formed the basis of the report. Wherever possible, recommendations were based on existing recommendations or guidelines. Where adequate guidelines did not exist, the guidelines were based on CDC experience and expertise.
This revised version is intended to more broadly address public health concerns related to limiting exposure to mold and identifying, preventing, and managing mold-related health effects following any natural disasters or other occurrences that results in flooding or major water intrusion. Published guidelines, established standards, and the peer-reviewed literature were reviewed to ensure the accuracy and consistency of the recommendations. In addition, the document was sent for stakeholder review and external peer review by experts in the areas of worker protection, general public health, medical, environmental and occupational epidemiology, allergy, industrial hygiene, mycology, and pulmonology.
Mold: A Definition
Molds, mushrooms, mildews, and yeasts are all classified as fungi, a kingdom of organisms distinct from plants and animals. Fungi differ from plants and animals in several respects. Unlike animals, fungi have cell walls. However, unlike plants, which also have cell walls, fungal cell walls are made mostly of chitin and glucan. Fungi cannot produce their own nutrients as plants do through photosynthesis. Fungi secrete enzymes that digest the material in which the fungi are imbedded and absorb the released nutrients. Multicellular fungi do not differentiate into different organs or functional components the way plants and animals do (5).
Approximately 100,000 species of fungi exists; fewer than 500 fungal species have been described as human pathogens that can cause infections (5). Visible growth of multicellular fungi consisting of branching filamentous structures (mycelia) are known popularly as molds (5) and are referred to by that term in this report.
Molds are ubiquitous in nature and grow almost anywhere indoors or outdoors. The overall diversity of fungi is considerable. For example, the genus Aspergillus has at least 185 known species (6). Molds spread and reproduce by making spores, which are small and lightweight, able to travel through air, capable of resisting dry, adverse environmental conditions, and capable of surviving a long time. The filamentous parts of mold (hyphae) form a network called mycelium, which is observed when a mold is growing on a nutrient source. Although these mycelia are usually firmly attached to whatever the mold is growing on, they can break off, and persons can be exposed to fungal fragments. Some micro-organisms, including molds, also produce characteristic volatile organic compounds (VOCs) or microbial VOCs (mVOCs). Molds also contain substances known as beta glucans; mVOCs and beta glucans might be useful as markers of exposure to molds (7).
Some molds are capable of producing toxins (sometimes called mycotoxins) under specific environmental conditions, such as competition from other organisms or changes in the moisture or available nutrient supply. Molds capable of producing toxins are popularly known as toxigenic molds; however, use of this term is discouraged because even molds known to produce toxins can grow without producing them (6). Many fungi are capable of toxin production, and different fungi can produce the same toxin(6).
Factors That Produce Mold Growth
Although molds can be found almost anywhere, they need moisture and nutrients to grow. The exact specifications for optimal mold growth vary by the species of mold. However, mold grows best in damp, warm environments. The availability of nutrients in indoor environments rarely limits mold growth because wood, wallboard, wallpaper, upholstery, and dust can be nutrient sources. Similarly, the temperature of indoor environments, above freezing and below the temperature for denaturing proteins, can support mold growth, even if the actual temperature is not optimal (8).
The primary factor that limits the growth of mold indoors is lack of moisture. Substantial indoor mold growth is virtually synonymous with the presence of moisture inside the building envelope. This intrusion of moisture might be from rainwater leaking through faulty gutters or a roof in disrepair, from a foundation leak, from condensation at an interface (e.g., windows or pipes), or between a cold and a warm environment. Water also can come from leaks in the plumbing or sewage system inside the structure. Studies of mold growth on building materials, such as plywood, have found that mold grows on materials that remain wet for 48--72 hours (8). Flooding, particularly when floodwaters remain for days or weeks, provides an almost optimal opportunity for mold growth.
Mold exposure can produce disease in several ways. Inhalation is usually presumed to be the most important mechanism of exposure to viable (live) or nonviable (dead) fungi, fungal fragments or components, and other dampness-related microbial agents in indoor environments. The majority of fungal spores have aerodynamic diameters of 2--10 µm, which are in the size range that allow particles to be deposited in the upper and lower respiratory tract (5). Inhalation exposure to a fungal spore requires that the spore be initially aerosolized at the site of growth. Aerosolization can happen in many ways, ranging from disturbance of contaminated materials by human activity to dispersal of fungi from contaminated surfaces in heating, ventilating, and air-conditioning (HVAC) systems. Fungal spores also can be transported indoors from outdoors. Overall, the process of fungal-spore aerosolization and related issues (e.g., transport, deposition, resuspension, and tracking of fungi to other areas) are poorly understood.
Persons can be exposed to mold through skin contact, inhalation, or ingestion. Because of the ubiquity of mold in the environment, some level of exposure is inevitable. Persons can be exposed to mold through contact with airborne spores or through contact with mycelial fragments. Exposure to high airborne concentrations of mold spores could occur when persons come into contact with a large mass of mold, such as might occur in a building that has been flooded for a long time. Exposure to mycelia fragments could occur when a person encounters a nutrient source for mold that has become disrupted, such as would occur during removal of mold-contaminated building material. Skin contact or exposure by inhalation to either spores or mycelial fragments also could occur in a dusty environment, if the components of dust include these fungal elements.
For the majority of adverse health outcomes related to mold exposure, a higher level of exposure to living molds or a higher concentration of allergens on spores and mycelia results in a greater likelihood of illness. However, no standardized method exists to measure the magnitude of exposure to molds. In addition, data are limited about the relation between the level of exposure to mold and how that causes adverse health effects and how this relation is affected by the interaction between molds and other microorganisms and chemicals in the environment. For this reason, it is not possible to sample an environment, measure the mold level in that sample, and make a determination as to whether the level is low enough to be safe or high enough to be associated with adverse health effects.
Persons affected by major hurricanes or floods probably will have exposure to a wide variety of hazardous substances distributed by or contained within the floodwater. This report does not provide a comprehensive discussion of all such potential hazards; such situations will of necessity require case by case evaluation and assessment. Guidance has been provided by CDC for such issues in a number of documents, including NIOSH Hazard Based Interim Guidelines: Protective Equipment for Workers in Hurricane Flood Response (9) and the CDC guidance: Protect Yourself From Chemicals Released During a Natural Disaster (10).
Factors That Cause Disease from Mold
Numerous species of mold cause infection through respiratory exposure. In general, persons who are immunosuppressed are at increased risk for infection from mold (11). Immunosuppression can result from immunosuppressive medication, from medical conditions and diseases that cause immunosuppression, or from therapy for cancer that causes transient immunosuppression. Although certain species of mold cause infection (5,8,11), many mold species do not cause infection. Infections from mold might be localized to a specific organ or disseminated throughout the body.
Many of the major noninfectious health effects of mold exposure have an immunologic (i.e., allergic) basis (6). Exposure to mold can sensitize persons, who then might experience symptoms when re-exposed to the same mold species. For sensitized persons, hay fever symptoms and asthma exacerbations are prominent manifestations of mold allergy (6). Although different mold species might have different propensities to cause allergy, available data do not permit a relative ranking of species by risk for creating or exacerbating allergy. In addition, exposure to beta glucans might have an inflammatory effect in the respiratory system (12).
Prolonged exposure to high levels of mold (and some bacterial species) can produce an immune-mediated disease known as hypersensitivity pneumonitis (13). Clinically, hypersensitivity pneumonitis is known by the variety of exposures that can cause this disorder (e.g., farmer's lung, woodworker's lung, and malt worker's lung).
Ingesting toxins that molds produce can cause disease. Longterm ingestion of aflatoxins (produced by Aspergillus species) has been associated with hepatocellular cancer (14). In addition, ingestion of high doses of aflatoxin in contaminated food causes aflatoxicosis and can result in hepatic failure (11). Whether concentrations of airborne mold toxins are high enough to cause human disease through inhalation is unknown, and no health effects from airborne exposure to mold-related toxins are proven.
Assessing Exposure to Mold
Any structure flooded after hurricanes or major floods should be presumed to contain materials contaminated with mold if those materials were not thoroughly dried within 48 hours (15,16). In such cases, immediate steps to reduce the risk for exposure to mold are likely to be of greater importance than further exposure assessment steps presented below.
Assessing the level of human exposure to mold in flooded buildings where mold contamination is not obvious is often a central and ongoing activity in recovery related to hurricanes and floods. Understanding the strengths and limitations of the approaches that are available to assess such exposures is important. Buildings that were not flooded could also have mold. For example, buildings with leaking roofs or pipes, which allows water to penetrate into biodegradable building materials, or excessive humidity, particularly buildings built with biodegradable materials, are susceptible to mold growth (2).
Visual Inspection and Moisture Assessment
A visual inspection is the most important step in identifying possible mold contamination (17,18). The extent of any water damage and mold growth should be visually assessed. This assessment is particularly important in determining remedial strategies and the need for personal protective equipment (PPE) for persons in the contaminated area. Ceiling tiles, gypsum wallboard (sheetrockTM), cardboard, paper, and other cellulosic surfaces should be given careful attention during a visual inspection. Not all mold contamination is visible (9,16); with a flood, contamination in the interior wall cavities or ceiling is common. A common means of assessing the mold contamination of a building is to estimate the total square feet of contaminated building materials (9,18,19). However, professional judgment will necessarily play an important role in the visual inspection because less quantifiable factors (e.g., location of the mold, building use, and function) and exposure pathways are also important in assessing potential human exposure and health risks.
Ventilation systems also should be visually checked, particularly for damp filters, damp conditions elsewhere in the system, and overall cleanliness. To avoid spreading microorganisms throughout the building, HVAC systems known or suspected to be contaminated with mold should not be run. Guidelines from the U.S. Environmental Protection Agency (EPA) and CDC (20,21) provide useful information concerning this topic. Different algorithms for assessing and remediating mold-contaminated buildings are available. Examples of such algorithms are available from the U.S. Army (22), the New York City Department of Health (18), and OSHA (23).
Moisture meters provide qualitative moisture levels in building materials and might be helpful for measuring the moisture content in a variety of building materials (e.g., carpet, wallboard, wood, brick, and concrete) following water damage (9,17). Meters also can be used to monitor progress in drying wet materials. Damaged materials should be removed and discarded. Moisture meters are available from contractor tool and supply outlets. Humidity meters can be used to monitor indoor humidity. Inexpensive (<$50) models that monitor both temperature and humidity are available.
A borescope is a hand-held tool that allows users to see hidden mold problems inside walls, ceiling plenums, crawl spaces, and other tight areas (6,18). No major drilling or cutting of dry wall is required.
Sampling for Mold
Sampling for mold is not part of a routine building assessment (9,16,18,19). In most cases, appropriate decisions about remediation and the need for PPE can be made solely on the basis of visual inspection. If visible mold is present, then it should be remediated regardless of what types of microorganisms are present, what species of mold is present, and whether samples are taken. Other than in a controlled, limited, research setting, sampling for biologic agents in the environment cannot be meaningfully interpreted and would not substantially affect relevant decisions about remediation, reoccupancy, handling or disposal of waste and debris, worker protection or safety, or public health. If sampling is being considered, a clear purpose should exist. For example:
To help evaluate a source of mold contamination. For example, testing the types of mold and mold concentrations indoors versus outdoors can be used to identify an indoor source of mold contamination that might not be obvious on visual inspection.
To help guide mold remediation. For example, if mold is being removed and it is unclear how far the colonization extends, then surface or bulk sampling in combination with moisture readings might be useful.
Types of Samples. Types of samples used to assess the presence of mold and the potential for human exposure to mold in a water-damaged building include air samples, surface samples, bulk samples, and water samples from condensate drain pans or cooling towers. Detailed descriptions of sampling and analysis techniques have been published (6,17).
Among the types of samples, airborne sampling might be a good indicator of exposure from a theoretical point of view, particularly for assessing acute short-term exposures. However, in practice, many problems (e.g., detection problems and high variability over time) limit the usefulness of these types of samples for most biologic agents. If air sampling is conducted, personal measurements best represent the current exposure, although practical constraints might make personal sampling difficult. Therefore, area sampling is the most commonly performed type of air sampling used to assess bioaerosol exposure despite resultant uncertainty about how accurately the measurements reflect actual personal exposure.
One type of surface sampling is the sampling of settled dust. A theoretical advantage of settled-dust sampling is the presumed correlation of concentrations of fungi in the settled dust with chronic exposure to those fungi (17). However, surface sampling is a crude measure and will yield a poor surrogate for airborne concentrations (6,17). Results of surface sampling as a measure of exposure should be interpreted with caution. Bulk samples can provide information about possible sources of biologic agents in buildings and the general composition and relative concentrations of those biologic agents.
Assessment of Microorganisms. Two distinct approaches are used for evaluation of the presence of specific microbes: culture-based and nonculture-based. The strengths and limitations of the different approaches have been published(6).
Instead of measuring culturable or nonculturable fungi or fungal components, constituents or metabolites of microorganisms can be measured as a surrogate of microbial exposure. Examples of such techniques include polymerase chain reaction (PCR) technologies and immunoassays (6,17). Methods for measuring microbial constituents (with some exceptions) are in an experimental phase and have not yet been routinely applied in clinical assessments, risk assessments, or epidemiologic studies.
No health-based standards (e.g., OSHA or EPA standards) or exposure limits (e.g., NIOSH recommended exposure limits) for indoor biologic agents (airborne concentrations of mold or mold spores) exist. Differences in season; climatic and meteorological conditions; type, construction, age, and use of the building and ventilation systems; and differences in measurement protocols used in various studies (e.g., viable versus nonviable microorganism sampling, sampler type, and analysis) make it difficult to interpret sampling data relative to information from the medical literature (6,17).If sampling is performed, exposure data can be evaluated (either quantitatively or qualitatively) by comparing exposure data with background data, indoor environments with outdoor environments, or problem areas with nonproblem areas. A quantitative evaluation involves comparing exposures, whereas a qualitative evaluation could involve comparing species or genera of microorganisms in different environments. Specifically, in buildings without mold problems, the qualitative diversity of airborne fungi indoors and outdoors should be similar. Conversely, the dominating presence of one or two kinds of fungi indoors and the absence of the same kind outdoors might indicate a moisture problem and degraded air quality. In addition, the consistent presence of fungi such as Stachybotrys chartarum, Aspergillus versicolor or various Penicillium species over and beyond background concentrations might indicate a moisture problem that should be addressed (17). Indoor and outdoor mold types should be similar, and indoor levels should be no greater than levels outdoors or in noncomplaint areas (17). Analytical results from bulk material or dust samples also might be compared with results of similar samples collected from reasonable comparison areas.