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Proceedings: Indoor Air 2002

HEALTH EFFECTS OF INDOOR FUNGAL EXPOSURE

F Fung1,2* and WG Hughson2

1 Sharp Rees-Stealy Medical Group, San Diego, CA, USA 2 UCSD Center for Occupational & Environmental Medicine, University of California, San Diego, CA, USA

ABSTRACT Objective To review current data on the health effects of indoor fungal bioaerosol exposure based on published studies. Methods We conducted MEDLINE search and reviewed all English language studies on indoor exposure (visible survey or objective sampling) and human health effects published from 1966 to January 2002. Main findings of the studies are analyzed in conjunction with plausible association of health effects and fungal exposure. Results Five case control studies, 16 cross-sectional surveys and 7 case reports met the selection criteria. Current evidence suggests that excessive moisture promotes mold growth and is associated with an increased prevalence of symptoms due to irritation, , and infection. However, specific toxicity due to inhaled fungal toxins has not been scientifically established. Conclusions Methods for assessing exposure and health effects are not well standardized, making interpretation of existing data difficult. Additional studies are needed to document human exposure- and dose-response relationships.

INDEX TERMS , , mold, allergy, .

INTRODUCTION Indoor air quality (IAQ) concerns are important public health issues. While acceptable IAQ has been addressed (ASHARE 1999), environmental health professionals and engineers are increasingly being asked to evaluate situations possibly associated with indoor pollutant exposure. This paper reviews and summarizes the current data linking human health effects to exposure.

METHODS We conducted a computerized search of MEDLINE database using the keywords bioaerosol(s), mold, , , dampness, indoor, indoor environment, health effects, respiratory, and sick building to find English language studies in the PubMed database published between 1966 and January 2002. The search yielded a total of 416 articles. Only human studies related to bioaerosol exposure from fungal sources were included in the selection process. Bioaerosol sampling methodology, mite, insect, animal dander, , plant and non-human studies were excluded. All original articles were obtained and reviewed for study purpose, methodology, exposure assessment, results and conclusions.

RESULTS Of the 416 published papers retrieved from the search, five are case-control studies. Three articles studied the possible association of chartarum exposure and the development of pulmonary hemorrhage in 10 infants living in the Cleveland area. Preliminary

* Contact author: Frederick Fung email [email protected]

46 Proceedings: Indoor Air 2002 data appeared to show a risk to infants living in water-damaged houses with Stachybotrys exposure. Environmental tobacco smoke was also a risk factor. However, after conducting further analysis, the Centers for Disease Control reported that the association between and pulmonary hemorrhage was not proven (MMWR 2000). One European case-control study assessed moisture and visible mold in the homes of 102 asthmatic patients. 196 subjects without served as controls. The study showed an increased prevalence of moisture and mold problems in the homes of asthmatic patients compared with controls. A study of 259 children with asthma or respiratory symptoms found an increase in dust mite and mold sensitization, and a greater prevalence of mold and water problems in the home, compared to 257 children who had no respiratory symptoms.

Sixteen cross-sectional studies were identified. These studies used either questionnaire or symptom survey tools to obtain information on mold. Most provided no specific diagnosis or case definition. A few studies utilized surface and/or air sampling for mold. There were no standardized methods for collection and quantification of the sampling data. Often, these studies evaluated multiple possible associations, increasing the likelihood that at least some statistically positive results would occur on a random basis. Nevertheless, many concluded that there was an association between respiratory symptoms and putative indoor fungal exposures. Despite significant limitations, these studies suggest a trend toward increased respiratory symptoms among those who occupied houses and buildings containing excessive moisture. An association between indoor mold and respiratory symptoms is also suggested.

Currently, there are 7 case reports associating indoor bioaerosols and mold with adverse health effects. There are 2 asthma case reports, two reports of ill-defined symptoms, and three reports of infants with pulmonary hemorrhage/hemosiderosis. Four recent reports indicate that the patients recovered completely after treatment or removal from further mold exposure. The tables summarize published human studies and reports on indoor mold and health effects.

Table1. Summarizes published case-control studies related to human health effects. Reference Setting Exposure Findings Comments assessment

CDC, Montana, 10 infants with Air and surface OR: smoking Association of mold growth Etzel (1997, acute pulmonary sampling for mold household 7.9, water- in water-damaged homes and 1998) hemorrhage/ damaged house 16.9, acute pulmonary hemorrhage hemosiderosis presence of S. atra 1.6 Williamson 102 asthmatics Dampness survey OR: 1.9 current, 2.1 Association of dampness and (1997) and 196 control of moisture and previous dampness. mold with asthma based on subjects visible mold r=0.3 for dampness severity score and spirometry and 0.23 for mold Verhoeff (1995) 259 children with Signs of home OR: 1.98 for reported Association of damp asthma or chronic dampness or mold dampness, 2.07 for house/mold and asthma or cough symptoms by questionnaire reported mold chronic cough and 257 controls and home visit

47 Proceedings: Indoor Air 2002

Table 2. Summarizes published cross-sectional studies related to human health effects. Reference Setting Exposure assessment Findings Comments

Jarvis 488 Visual, air and surface Increase rates of symptoms Symptom rates remained (2001) building sampling with moisture and mold unchanged after remediation occupants upon re-occupancy

Ross 57 Air sampling for mold Association of ER visits with Increase in asthma severity (2000) asthmatic and dust sampling for total and Gram(-) bacteria indicators. No control subjects adults mite antigen and total mold

Dales 403 History of mold 12-50% increase in Mold was not sampled. No (1999) elementary growth, air sampling of respiratory symptoms specific diagnosis was made school bacterial endotoxin and associated with mold growth children mite antigen

Jedrychow- 1129 Outdoor air pollutant Presence of mold or Symptoms survey. No ski (1998) school sampling and history of dampness is associated with objective measure of mold children indoor dampness/mold hay fever, wheezing and problems. difficulty breathing

Hodgson 14 adults Site evaluation, air and Possible/likely building- Presumed mycotoxin-induced (1998) surface sampling for related asthma, and effects. Case definition unclear. mold interstitial lung disease (ILD) No X-ray evidence of ILD.

Sudakin 37 adults Site evaluation, air and High prevalence of multiple Evidence of fungal (1998) surface sampling for symptoms, neurobehavioral (Penicillium, Aspergillus) and mold and bacteria and upper respiratory bacterial growth. Symptoms complaints. less prevalent after relocation

Li (1997) 264 day- Site evaluation, air and High prevalence of “sick- Symptom survey only. No care surface sampling for building syndrome” specific diagnosis made. workers mold, bacteria, dust exposure to dampness and mite Aspergillus

Yang 4164 Questionnaire survey Association of cough, Survey of health and exposure (1997) school of home dampness, wheeze, bronchitis, asthma by self-reported questionnaires children mold or flooding with dampness

Johanning 53 office Air and surface/bulk Subjective respiratory/ other No sampling of the control (1996) workers sampling for mold and symptoms associated with environment. No specific mycotoxin mold diagnosis made.

Cuijpers 470 school Questionnaire survey Damp stains and mold Statistically significant (1995) children of indoor growth are associated with association of asthma-like environmental factors chronic cough symptoms with passive smoking, but not mold growth

Dales 14799 Questionnaire survey Dampness/ mold were Self reported symptoms and (1991) adults of home dampness/ associated with respiratory visible mold mold symptoms

Dales 13495 Same methodology and Respiratory symptoms were Self reported symptoms and (1991) children data base as above more prevalent in homes visible mold by with /dampness parents/guardians

Strachan 1000 Questionnaire survey Association of excess Sterile mycelia were higher in (1990) children symptoms/ dampness wheeze and moldy/damp homes of wheezy children. Air and visible mold, air homes. sampling showed mold levels sampling followed varied widely between houses.

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Reference Setting Exposure assessment Findings Comments

Brunekreff 4625 Questionnaire survey Increase in respiratory Self-reported symptoms and (1989) children symptoms, dampness symptoms and dampness/visible mold and visible mold dampness/mold

Platt (1989) 579 Assessment of Association of respiratory Greater prevalence of households dampness/mold and symptoms with damp/ moldy symptoms among children. health interview homes

Waegemae 519 adults, Questionnaire and air Damp homes had higher rate Higher mold counts in kers (1989) children sampling viable mold of respiratory symptoms damp homes OR: Odds ratio; r: correlation coefficient

Table 3. Summarizes published case reports related to human health effects. Reference Setting Exposure Assessment Findings Comments

Trout (2001) Worker with Air and surface Identification of Unclear medical diagnosis. hypersensitive (?) sampling Penicillium, Serology was not useful in respiratory illness Aspergillus and identifying exposure Stachybotrys sp. Novotny Infant Pulmonary Air and surface Isolation of surface Patient remained clinically (2000) hemorrhage sampling for mold Penicillium and healthy after discharge Trichoderma Fung (2000 ) Asthmatic adult Air and surface (+) in vitro/in vivo Patient recovered with sampling for mold test for Alternaria treatment and after fungal source was remediated Elidemir Infant with Surface sampling for S. atra, Aspergillus S. atra was recovered from (1999) Pulmonary mold and Penicillium were BAL. Patient recovered hemorrhage recovered completely

Flappan Infant with Air and surface Stachybotrys spores Mycotoxin was found in mold (1999) Pulmonary sampling for mold found in air sampling contaminated area hemorrhage Croft( 1986) 4 family Fungal spores by "Flu" symptoms. S. No objective evidence of members and a impinger sampling. atra extracts found in specific disease detected. No maid Ceiling and dust ceiling and duct dust further complaints after house samples for mold were toxic to animals was cleaned Kozac(1980 ) 7 children with Viable, non-viable Clinical evidence of Possible allergy to various asthma and/or spores, direct tape and allergy and asthma. 1 fungi including Stachybotrys allergy bulk sample for mold child had positive skin prick for S. atra

DISCUSSION Building related complaints include diverse symptoms reported by occupants as the result of chemical, physical and biological exposures in the indoor environment. Except for specific chemical or toxic gas exposures such as carbon monoxide, building related illnesses are usually associated with exposure to bioaerosols (Macher 1987). Bioaerosols can cause four types of human illness: allergy, infection, irritation and toxicity. Allergy and hypersensitivity such as , asthma and hypersensitivity pneumonitis result from exposure to allergens that stimulate specific immunological responses. Infection refers to the entry and multiplication of a biological agent in a host’s body. The most common fungal disease is superficial mycosis, such as tinea infection. Irritation due to bioaerosol

49 Proceedings: Indoor Air 2002 exposure may result in conjunctivitis, rhinitis and asthma. Mold can produce a variety of organic chemicals that produce typical musty and pungent odors. Glucans are glucose polymers found in most fungal cell walls. Exposure to airborne (1Æ3) beta-D-glucan has been associated with airway (Rylander 1997). Toxicity due to fungal exposure is caused by mycotoxins produced by molds (Fung 1998). Documenting toxic effects from any mycotoxin should include (a)presence of airborne spores containing toxin; (b)levels of toxin exposure sufficient to cause disease; (c)observed health effects related to toxin exposure rather than other mold components. Although cancer has been associated with ingestion of mycotoxins, current evidence indicates that cancer due to inhaling mycotoxin requires chronic exposure in heavily contaminated industrial environments.

CONCLUSIONS AND IMPLICATIONS Health effects caused by bioaerosol exposure from fungal sources include allergy, infection, irritation and toxicity. Current published human studies demonstrate an association of allergy and respiratory symptoms, and exposure to moisture/mold. While the first three categories have well established mechanisms, there is a lack of dose-response data, and a highly variable degree of individual susceptibility. Specific toxicity due to inhaled mycotoxins is not well documented, and remains controversial. In the absence of specific illness and respiratory symptoms among the occupants of a home or office, caution is warranted in responding to visible mold with knee-jerk advice such as, “Move out of your house” or “Evacuate the building,” since such actions would have significant psychosocial and economic consequences. Excessive moisture is a risk factor for mold proliferation, it therefore, is prudent to identify the source of moisture, and then repair and fix water intrusion problems before starting an expensive and usually low-yield environmental investigation. The methods for assessing and controlling bioaerosol exposures are based more on a consensus of researchers and practitioners rather than objective scientific data (ACGIH 1999). Future research in bioaerosol should include standardizing protocol for assessment and control based on best available scientific evidence; identification of specific components that define clinical disease; and development of a validated biomarker for fungal bioaerosol exposure.

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