Introduction by Eckardt Johanning, M.D., M.Sc. Conference Director

Fungi in indoor environments - a challenge for scientific research and public health

This book contains the proceedings of the Third International Conference on Fungi, Mycotoxins and Bioaerosols - Health effects, Assessment, Prevention and Control, a scientific meeting that brought together physicians, veterinarians, industrial hygienists, mycologists, chemists, public health specialists, toxicologists, and laboratory specialists among many others. Four years have passed since our first International Conference in Saratoga Springs, New York: Fungi and Bacteria in Indoor Air Environments in fall of 1994 (Johanning and Yang, 1995). Again, we gathered a wide range of health professionals, indoor air consultants, research scientists and policy makers from universities and governmental agencies, such as Environmental Protection Agency (EPA), National Institute for Occupational and Environmental Health (NIOSH) and the Department of Health (DOH) - and last but not least the stake holders: representatives of patients, insurance companies, building managers, lawyers and unions to present new research results and to discuss the health implications of microbials in indoor environments or industries. Following our second meeting in 1996 that focused more on specific technical issues related to microbial remediation in buildings, we felt it was again time to get together, to talk and to compare notes about this theme that has become such a “hot topic“ for the scientific community, but also for the public and the media. It became truly an international meeting with almost 350 people, and about half of the participants coming from around the world, from Belgium, Canada, Denmark, Finland, Germany, Japan, Netherlands, Norway, Slovakia, South Africa, Sweden and other countries - with more than 90 original presentations on the health effects, assessment, prevention and control of bioaerosols, fungi and mycotoxins at home or in the workplace. The stated learning objectives were to

• Discuss current data and new information on exposure, assessment, analytical methods, applied research, pathology, epidemiology, microbiology, health effects, prevention and mitigation of bioaerosol exposure

• Recognize the importance of bioaerosol exposure and adverse health effects

• Develop a multi-disciplinary team approach for the recognition and management of bioaerosol exposure.

This meeting has become recognized as a unique forum to present original research to a critical peer-audience, to discuss public health policies, but also to review concrete technical issues about detection and control of fungi and bacteria in our environment. The presented papers and scientific debate also showed that this is a topic of international concern. It crosses national barriers and affects different climatic zones. Since our first meeting in 1994 there is hardly any professional conference meeting on indoor air quality and health issues that does not mention moisture and water damage-related mold problems in buildings. The apparent widespread nature of the problems and the far reaching public health implications are gaining wider recognition among professionals and the lay public, but surely not without controversies and conflict of interest in some cases.

The scope and the numbers

The ‘ingredients’ for problems with unusual microbial exposure inside buildings appear readily available in many places and affect a wide range of people: water and organic building materials (cellulose). In other words: Moisture and condensation problems, water pipe leaks, flooding and storm-related defects, occurring in buildings and homes with wood, paper sheeted gypsum board or fiberglass insulation, carpets and furniture can result in significant microbial contamination if the water intrusion is neglected. Furthermore, many old and new industries are exposing workers to fine organic dust (microbial materials that become airborne) due to increased mechanized processing or handling of recyclable organic materials and waste that should not end up in landfills. A wide range of workers in various industries is potentially at risk for high exposure to microbials (fungi, bacteria, viruses) or its products (allergens, endotoxins, glucans, mycotoxins).

Number of workers in different industries with potentially significant microbial exposures:

            Industry: (No. of workers with “organic dust“ exposure:)

•           Farming (1.3 Mill.)

•           Lumbar/Wood (818000)

•           Food (1.7 Mill.)

•           Textile mills (590000)

•            Paper production (682000)

•            Agricultural service (786000)

•            Museum, Botanical and Zoological gardens (98000)

•            Garden/Building material (1 Mill.)

A number of health problems related to moisture defects in buildings and occupational exposure to organic type of dust has been clinically observed. These have been coined a new challenge to occupational medicine (Reijula 1996. Johanning et al. 1998). Nevertheless, the inhalation of organic dust, defined as dust of vegetable, animal, or microbial origin, and related diseases has been well recognized and described earlier. However, it was thought to be mainly related to agricultural and farming activities (cotton processing, handling of animals, grain and food. But now we begin to recognize that also in non-agricultural environments significant exposure may occur accidentally. Two publications have well documented some of these earlier findings by various investigators in the agricultural and indoor environment (Rylander and Jacobs, 1994; Samson et al. 1994).

We are learning now that excessive exposure to such ‘organic dust’ can principally also occur in indoor environments and that chronic moisture problems may be very common in many buildings. Most of us spend the greater part of our lives inside buildings and vehicles - and depend more often on mechanical ventilation for “fresh air“, heat, cold and moisture. The emphasis on the reduction of building costs and maintenance, and the need for energy conservation has resulted in “tighter“ buildings that appear to be more prone to aging-related defects and system failures. In our experience, all too often, current building technology and management do not satisfy our needs for “good air quality“, free of harmful pollution or even for general comfort. The reason for most ventilation failures and problems are often not complicated and easily correctable, as EPA and NIOSH studies have shown. “Sick building“-related health complaints by our patients are very common, in particular in the occupational and environmental health clinics. Some medical sociologists suggest that indoor air quality (IAQ)-related complaints and diseases will be with us long into the next millennium and will gain greater importance than traditional chemical poisoning of industrial workers. Although our understanding of the multiple factors and their effects on air quality has increased considerably in the last decades there still remains a number of unanswered questions and scientific puzzles. Nevertheless, many of us IAQ experts believe, that if what we know now about tobacco smoke, volatile organic compounds, fibers, HVAC-systems, air pollution, etc. were applied and already-existing recommendations and standards were followed by the responsible parties, then most of the IAQ complaints would be resolved and the need for medical intervention would be substantially reduced.

However, there is still quite a task ahead of us and the numbers are impressive. In the U.S., of the total employed population of 131.2 Mill., approximately 70 Mill. people work indoors. In 1989 there were about 4.5 Mill. commercial buildings in the U.S. (28% service/shops, 15% offices, 14% assembly warehouses, 5% food services, 3% lodging and 2% food sales/health services). The Occupational Safety and Health Administration (OSHA) reported in the 1994 Indoor Air Quality (IAQ) proposal for a regulatory standard, that 30% of the 70 Mill. “indoor“ workers have poor air quality (Federal Register, 1994). The National Institute for Occupational Safety and Health (NIOSH) reported that based on their review of previous health hazard evaluations (HETA) related to building/facility problems 42% of 104 buildings investigated had evidence of “water damage“ (Crandall et al. 1996).

How healthy are our school buildings?

Our children and teachers spend a considerable portion of their life inside school buildings that are aging and often in need of repair. A recent governmental investigation revealed that of the more than 80000 schools in U.S., one third of them is in need of extensive repairs costing about 112 billion (GAO/HE’S, 1995):

•          14 Mill. students affected

•          50% of the surveyed schools reported „unsatisfactory environmental conditions:

            Problem:        No. of schools No. of students

            Ventilation        21100            11.6 Mill.

            Heating            15000            7.8 Mill.

            Indoor air quality            15000            8.4 Mill.

Many schools and colleges have water leaks and mold problems, which are now increasingly monitored by local and state health departments, teachers’ unions, i.e., the American Federation of Teachers (Washington, D.C.) and parents’ organizations.

What about the indoor environmental quality in private homes in the U.S.?

Here are the statistics: There are 94,7 Million households or units in U.S. for the U.S. population of 270,5 Mill.:

•          61 Mill. owner occupied

•          33 Mill. renter occupied

•          59 Mill. single structures.

Of these homes, 47 Mill. were built between 1959 and 1975. The median age of the homes is 30-40 years. According to a U.S. government statistic, many of the buildings have leakage problems. Water leakage during last 12 months(U.S. Census, 1998 (most recent available statistics)):

•          10.9 Mill. (13%) U.S. homes had leakage from inside

            •            3.8 Mill. (34%) Fixture backups/overflow

            •            5.1 Mill. (46%) Pipe leaks

•          16.9 Mill. (21%) U.S. homes had leakage from outside

            •            7.1 Mill. (42%) roof

            •            6.1 Mill. (36%) basements

            •            3.0 Mill. (18%) walls.

In this context, it may come as no surprise that of the 9.7 Mill. owner-occupied units surveyed the most frequent repair within the prior two year period was: Roof repair (!), followed by building of additions, kitchen or bath remodeling/adding, siding replacement, etc. What does that tell us about the status and quality of the U.S. housing stock and the possibility of water intrusion and subsequent microbial growth?

Another source of “moisture“ which is an important factor in indoor mold growth is heavy rains and flooding. During the spring of 1993, with the now called Great Mississippi Flood, flooding of 11,000,000 acres of land occurred - this is about one quarter of land area of the continental United States (see also: www.earthsat.com). Since then more widespread and recurrent flooding has occurred in many different parts of the U.S., often affecting the housing and causing substantial damage. A rapid cleanup of water-damaged homes can help to minimize widespread microbial problems, but special precautions and adequate personal protective equipment are recommended by official agencies (FEMA, 1997). It appears that a considerable number of children and adults in these are affected by allergy, asthma and other disorders as a result of it. The true impact of these natural disasters and mold problems on the public health in these areas has not been systematically studied, although this would be an important project for prevention.

Fungi and health

The possible pathological consequences in humans and animals of exposure to bacteria and fungi fall principally into the categories of infection, allergy, and toxicity (Husman, 1996, Johanning 1999). In clinical practice the overlap of these pathological reactions of fungi is quite common. This may explain the wide variety of medical presentations and findings and why so many different medical specialties are involved in the care of such patients. Many medical providers, however, still have very little knowledge and training about air contamination problems and building-related diseases. This leads to delay in proper diagnosis and treatment failure, because the underlying causes are not recognized or evident problems with the IAQ (or now redefined as: Indoor environmental quality (IEQ)) are not corrected. Surely, a healthy individual with a good functioning immune system and respiratory organs should be able to handle most temporary adverse situations with IEQ problems, without any (lasting) harm and subsequent physical impairment. Many physicians are familiar with the concept of allergy and infection caused by fungal exposure, but irritative and toxic effects caused by fungi (or gram negative bacteria) in the form of inhalation of microbial by-products such as endotoxins, glucans and mycotoxins are still not widely known.

Mycotoxin-related diseases, life stock illnesses and death, and economic losses are very familiar to veterinarians and food safety specialists. References to the effects of a wide range of mycotoxins and other fungal-by-products can be found in medical sub-specialty fields. In the past, mycotoxins, which are naturally occurring chemical metabolites of fungi, have been implicated in cases of food poisoning, but research has shown that inhalation of mycotoxin-loaded spores and mycilia may have even greater potency and may be of concern for the individual with intense or prolonged exposures. Some of the now known and studied mycotoxins (there are several hundred different types) have been shown to have biological effects in humans and animals with various degrees of acute and chronic toxicity, cytotoxity, neurotoxicity, immunosuppressive effects, teratogenicity, mutagenicity, carcinogenicity, anti-tumor effects, and adverse endocrinologic effects. But much of this research has been done under laboratory conditions and little is still known about its impact in indoor environments and under “real-life“ conditions when several fungal agents are present. However, past medical research has shown, that certain mycotoxins are able to target and adversely affect many body organs or systems, such as the lungs, skin, mucous membranes, the central and peripheral nervous system, the immune system (white blood cells), the liver, and the cardiovascular system and consequently cause a wide range of symptoms. On a molecular level they can interact and interfere with the DNA and RNA replication, transcription and translation, causing protein synthesis defects and inhibition, cell membrane defects and energy metabolism errors (Betina, 1989; Sharma RP and Salunkhe DK, 1991). Because of the unique potent effects of a few mycotoxins in humans and animals, they have been studied in many applications, from cancer chemotherapy to biological warfare research. Mycotoxins are considered important environmental pollutants. Small amounts of these compounds may result in serious health hazards, i.e., intoxication, cancer and death (WHO, 1979, IARC, 1993), although in the past the ingestion route has been thought to be of greater importance in public health and food safety. More recent clinical-epidemiological cluster investigations of unusual disease outbreaks in homes, office buildings, court houses, and in the Cleveland area of lethal hemorrhagic lung diseases in infants have focused the attention on inhalation-related health risks of toxic fungi, such as Stachybotrys chartarum (a.k.a. atra), which may be more common and important in many cases of so-called “sick-building syndrome“ or certain building-related diseases (i.e., bronchitis, pneumonitis)(Auger et al. 1994; Johanning et al. 1996; Hodgson et al. 1998; Etzel et al. 1998, Johanning, 1998). Such problems and outbreaks have not been sufficiently studied and documented in the past due in part to complex methodological and technical problems. From a statistical perspective research involving several exposure agents and disease outcomes occurring in small populations is very difficult and involves many limitations.

The allergy and asthma ‘epidemic’

Nevertheless, several diseases of great public health importance are known to be either strongly associated, caused or substantially aggravated by exposure to fungi and microbial by-products, although the exact pathological mechanisms are still under investigation and often difficult to prove. One of these diseases is asthma, or more specifically occupational or environmental type asthma (Peat et al. 1998). In the USA there are about 12 Million people diagnosed with asthma. The numbers of recorded cases are steadily rising, with a jump of 29% between 1980 and 1987. There was also an increase in asthma-related deaths from 2000 per year reported for 1979 to 9394 in 1993. Besides the associated suffering in patients, the costs are enormous with an estimated $ 6.5 billion/year (medical expenses and indirect costs). It is estimated that about 40% may be saved with improved diagnosis and treatment, which also means better recognition of causes and exposure prevention. Occupational and environmental asthma is now the most common workrelated respiratory disorder (2% to 15% of all adultonset asthma). There are more than 450 substances in the workplace known to be associated with occupational asthma. Many of these are of biological origin, including fungi.

What about rhinitis and sinusitis, and plain allergy? Are these just “trivial“ conditions? If you are not yourself a “sufferer“- just look at the numbers to get an appreciation of the scale of the problems. The number of people with allergic conditions is generally on the rise and more and more of these patients take some form of allergy medication. It is not certain, whether this may be a real trend or just a reflection of improved diagnostic tests and more reporting.

            Allergic rhinitis statistic:

            •            30 to 40 Mill. people in U.S.

            •            19 Mill. employed adults

            •            3.5 Mill. lost workdays annually

            •            2 Mill. lost schooldays annually

            •            Direct costs: $2.4 billion

 

 

            Sinusitis statistic:

            •            35 Mill. (15%) people in U.S.

            •            25% and more are related to allergy

            Allergic rhinitis, sinusitis and asthma

            •            20 80% of patients have a combined diagnosis.

Clearly, many cases of respiratory diseases, allergy and asthma are probably of multi-factorial origin and many substances have been implicated as causes in addition to genetic factors and host susceptibility. But what is important in this context here, is that public health research suggests that many of these diseases and exposure conditions could principally be prevented. There is wide agreement among the experts that it is prudent to avoid and minimize unnecessary exposure to fungi or bacteria. In particular exposure to known infectious, allergenic, toxic and carcinogenic fungi (i.e., Aspergillus fumigatus, A. flavus, A. versicolor, Stachybotrys chartarum and possibly some other fungal species) should not be tolerated because of what we know about their possible deleterious effects on animals and humans - even if we still do not know exactly, when, how and why people get sick from inhalation (or skin contact) of these fungal species (see also the recent publication of a related workshop with the topic: Indoor mold and children’s health (Rylander and Etzel, 1999)).

In analogy to John Snow (a general practitioner in London, 1813-1858), who found out through pioneering simple epidemiological studies that the contaminated water made the people sick and advised to avoid certain water fountains in London, without initially knowing that it was the cholera microbe that caused the disease, it appears timely and prudent that public health advocates and agencies advise the public to follow the prudent hygiene principle: Do not live or work inside buildings with moisture and mold problems. Historically, this simple but “life saving“ advice may even be traced back to the final of the 10 plaques and the Egyptian exodus, as well as to writings in the bible and other religious scripts, as some scholarly historians say (The Sunday Times, Aug. 16th, 1998). Indeed the fungal “poisons of the past“ are thought to be the cause of the black plaque, the Salem witch-hunts, the “holy fire“ (bizarre behavior caused by ergotism) and there appears to be good evidence to suggest that fungal food poisoning with mycotoxins has been responsible for the reduced fertility and the high mortality in the past centuries in Europe and Russia, during a time when large populations relied heavily on food (bread) contaminated with mycotoxins (Matossian, 1989). Better nutrition and generally improved hygiene have resulted in a resolution of these problems and substantial gains in the public health status.

Improving the indoor air and building quality cannot be solved by medical means alone, but requires social, political and economical attention. Although the results of recent research activities and field experiences presented in this book have given us much greater insight into this scientific topic and the understanding of fungal and bacterial disease is improving, there are still many unanswered questions and a lot of work remains to be done. This will require continued research efforts and learning from field and laboratory studies, and dissemination of information in publications, professional meetings and continuous medical/professional education. Most of all, we will have to work as multi-disciplinary teams and independent studies with appropriate funding need to be conducted. The past conferences and this book are a demonstrated concerted effort to move in this direction.

As we said earlier in the proceedings of the first international meeting, the lay reader should be reminded to consider, that fungi and bacteria are ubiquitous and indeed part of our “normal“ life. The shear presence and detection of microbials in our immediate environment does not necessarily mean harm or that this will cause suffering or illnesses. Obviously most of us in the medical field think that healthy individuals should be able to “handle“ a certain amount of toxic or allergenic molds for brief periods without suffering any long-term harm and consequences, but we do not know for sure what are “safe“ exposure limits (such as used in the chemical field with so-called “permissible exposure limits (PELs)“) for various fungi or its by-products. Furthermore, medical tests are not readily available to diagnose mold-borne diseases and we are not able to provide “magic remedies“ other than advice about exposure cessation and give supportive measures (which incidentally has worked for most people - see Johanning and Landsbergis, 1999 in this book). We need to improve our understanding of atypical, unusual or abnormal conditions under which naturally occurring biological materials, such as fungi and bacteria, can turn out to be a significant health risk to humans or animals. And further, when does it deserve our attention or require medical and public health intervention? All this will require interdisciplinary professional team work, consensus development, and financial support - as well as an open and honest scientific debate. We hope that this conference and this book will serve as a basis for this - so that in the end our patients and public health will benefit from this cooperative effort.

Again, I wish to thank all of our supporters, the organizing committee and the organizations that gave us their endorsement:

References

• Auger PL, Gourdeau P, Miller JD. 1994. Clinical experience with patients suffering from a chronic fatigue-like syndrome and repeated upper respiratory infections in relation to airborne molds. Am J Ind Med 25(1):41-2.

• Betina V. 1989. Mycotoxins. Chemical, biological and environmental aspects. Bioactive molecules. Vol 9. Amsterdam/New York: Elsevier.

• Crandall MS, Sieber WK. 1996. The National Institute for Occupational Safety and Health Indoor Environmental Evaluation Experience. Part One: Building Environmental Evaluations. Appl Occup Environ Hgy 11(6):533-539.

• Etzel RA, Montaña E, Sorenson WG, Kullman GJ, Allan TM, Dearborn DG. 1998. Acute pulmonary hemorrhage in infants associated with exposure to Stachybotrys atra and other fungi. Arch Pediatr Adolesc Med 152:757-62.

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• FEMA. 1997. Federal Emergency Management Agency. (www.fema.gov).

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• The Sunday Times. 1998. One damned thing after another in ancient Egypt. (Research done by John Marr and Curtis Malloy). August 16th., London, UK.

• U.S. Census Bureau. 1998. American Housing Survey (AHS-N data charts from 1993 survey). Current housing reports, series H150/93. (www.census.gov/ftp/hhes/housing/ahs.).

• WHO (World Health Organization). 1979. Environmental Health Criteria, 11, Mycotoxins. World Health Organization, Geneva, Suisse.