HEALTH EFFECTS OF INDOOR FUNGAL BIOAEROSOL EXPOSURE

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1 HEALTH EFFECTS OF INDOOR FUNGAL BIOAEROSOL EXPOSURE F Fung 1,2* and WG Hughson 2 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 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 growth and is associated with an increased prevalence of symptoms due to irritation, allergy, and infection. However, specific toxicity due to inhaled fungal toxins has not been scientifically established. Conclusions Methods for assessing indoor bioaerosol exposure and health effects are not well standardized, making interpretation of existing data difficult. Additional studies are needed to document human exposure-disease and dose-response relationships. INDEX TERMS Bioaerosols, indoor air quality,, allergy, mycotoxins. 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 indoor exposure. METHODS We conducted a computerized search of MEDLINE database using the keywords bioaerosol(s),, fungus, mycotoxin, dampness, indoor, indoor environment, health effects, respiratory, and sick building to find English language studies in the PubMed database published between 1966 and January 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, dust mite, insect, animal dander, bacteria, 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 Stachybotrys chartarum exposure and the development of pulmonary hemorrhage in 10 infants living in the Cleveland area. Preliminary * Contact author: Frederick Fung fred.fung@sharp.com 46

2 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 Stachybotrys chartarum and pulmonary hemorrhage was not proven (MMWR 2000). One European case-control study assessed moisture and visible in the homes of 102 asthmatic patients. 196 subjects without asthma served as controls. The study showed an increased prevalence of moisture and problems in the homes of asthmatic patients compared with controls. A study of 259 with asthma or respiratory symptoms found an increase in dust mite and sensitization, and a greater prevalence of and water problems in the home, compared to 257 who had no respiratory symptoms. Sixteen cross-sectional studies were identified. These studies used either questionnaire or symptom survey tools to obtain information on. Most provided no specific diagnosis or case definition. A few studies utilized surface and/or air sampling for. 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 and respiratory symptoms is also suggested. Currently, there are 7 case reports associating indoor bioaerosols and 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 exposure. The tables summarize published human studies and reports on indoor and health effects. Table1. Summarizes published case-control studies related to human health effects. Reference Setting Exposure assessment CDC, Montana, Etzel (1997, 1998) Williamson (1997) Verhoeff (1995) 10 infants with acute pulmonary hemorrhage/ hemosiderosis 102 asthmatics and 196 control subjects 259 with asthma or chronic cough symptoms and 257 controls Proceedings: Indoor Air 2002 Air and surface sampling for Dampness survey of moisture and visible Signs of home dampness or by questionnaire and home visit Findings OR: smoking household 7.9, waterdamaged house 16.9, presence of S. atra 1.6 OR: 1.9 current, 2.1 previous dampness. r=0.3 for dampness and 0.23 for OR: 1.98 for reported dampness, 2.07 for reported Comments Association of growth in water-damaged homes and acute pulmonary hemorrhage Association of dampness and with asthma based on severity score and spirometry Association of damp house/ and asthma or chronic cough 47

3 Table 2. Summarizes published cross-sectional studies related to human health effects. Reference Setting Exposure assessment Findings Comments Jarvis (2001) 488 building occupants Visual, air and surface sampling Increase rates of symptoms with moisture and Symptom rates remained unchanged after remediation upon re-occupancy Ross (2000) 57 asthmatic adults Air sampling for and dust sampling for mite antigen Association of ER visits with total and Gram(-) bacteria and total spores Increase in asthma severity indicators. No control subjects Dales (1999) 403 elementary school History of growth, air sampling of bacterial endotoxin and mite antigen 12-50% increase in respiratory symptoms associated with growth Mold was not sampled. No specific diagnosis was made Jedrychowski (1998) 1129 school Outdoor air pollutant sampling and history of indoor dampness/ Presence of or dampness is associated with hay fever, wheezing and difficulty breathing Symptoms survey. No objective measure of problems. Hodgson (1998) 14 adults Site evaluation, air and surface sampling for Possible/likely buildingrelated asthma, and interstitial lung disease (ILD) Presumed mycotoxin-induced effects. Case definition unclear. No X-ray evidence of ILD. Sudakin (1998) 37 adults Site evaluation, air and surface sampling for and bacteria High prevalence of multiple symptoms, neurobehavioral and upper respiratory complaints. Evidence of fungal (Penicillium, Aspergillus) and bacterial growth. Symptoms less prevalent after relocation Li (1997) 264 daycare workers Site evaluation, air and surface sampling for, bacteria, dust mite High prevalence of sickbuilding syndrome exposure to dampness and Aspergillus Symptom survey only. No specific diagnosis made. Yang (1997) 4164 school of home dampness, or flooding Association of cough, wheeze, bronchitis, asthma with dampness Survey of health and exposure by self-reported questionnaires Johanning (1996) 53 office workers Air and surface/bulk sampling for and mycotoxin Subjective respiratory/ other symptoms associated with No sampling of the control environment. No specific diagnosis made. Cuijpers (1995) 470 school of indoor environmental factors Damp stains and growth are associated with chronic cough Statistically significant association of asthma-like symptoms with passive smoking, but not growth Dales (1991) adults of home dampness/ Dampness/ were associated with respiratory symptoms Self reported symptoms and visible Dales (1991) Same methodology and data base as above Respiratory symptoms were more prevalent in homes with s/dampness Self reported symptoms and visible by parents/guardians Strachan (1990) 1000 symptoms/ dampness and visible, air sampling followed Association of excess wheeze and y/damp homes. Sterile mycelia were higher in homes of wheezy. Air sampling showed levels varied widely between houses. 48

4 Reference Setting Exposure assessment Findings Comments Brunekreff (1989) 4625 symptoms, dampness and visible Increase in respiratory symptoms and dampness/ Self-reported symptoms and dampness/visible Platt (1989) 579 households Assessment dampness/ health interview of and Association of respiratory symptoms with damp/ y homes Greater prevalence of symptoms among. Waegemae kers (1989) 519 adults, Questionnaire and air sampling viable OR: Odds ratio; r: correlation coefficient Damp homes had higher rate of respiratory symptoms Higher spore counts in damp homes 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 Penicillium and healthy after discharge Trichoderma Fung (2000 ) Asthmatic adult Air and surface sampling for Elidemir (1999) Infant with Pulmonary hemorrhage Surface sampling for (+) in vitro/in vivo test for Alternaria S. atra, Aspergillus and Penicillium were recovered Patient recovered with treatment and after fungal source was remediated S. atra was recovered from BAL. Patient recovered completely Flappan (1999) Infant with Pulmonary hemorrhage Air and surface sampling for Stachybotrys spores found in air sampling Mycotoxin was found in contaminated area Croft( 1986) 4 family members and a maid Fungal spores by impinger sampling. Ceiling and dust samples for "Flu" symptoms. S. atra extracts found in ceiling and duct dust were toxic to animals No objective evidence of specific disease detected. No further complaints after house was cleaned Kozac(1980 ) 7 with asthma and/or allergy Viable, non-viable spores, direct tape and bulk sample for Clinical evidence of allergy and asthma. 1 child had positive skin prick for S. atra Possible allergy to various fungi including Stachybotrys 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 diseases such as rhinitis, 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

5 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 (1 3) beta-d-glucan has been associated with airway inflammation (Rylander 1997). Toxicity due to fungal exposure is caused by mycotoxins produced by s (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 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/. 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 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 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. REFERENCES American Conference of Governmental Industrial Hygienists, Inc Bioaerosols: Assessment and Control. J. Macher, Ed. ACGIH, Cincinnati, ASHRAE American Society of Heating, Refrigerating and Air-Conditioning Engineers.Ventilation for Acceptable Indoor Air Quality Standard Brunekreef B, Dockery DW, Speizer FE et al Home dampness and respiratory morbidity in. Am Rev Respir Dis 140: Croft WA, Jarvis BB, Yatawara CS Airborne outbreaks of trichothecene toxicosis. Atmospheric Environment 20: Cuijpers CE, Swaen GM, Wesseling G, et al Adverse effects of the indoor environment on respiratory health in primary school. Environ Res 68: Dales RE, Burnett R, Zwanenburg H Adverse health effects among adults exposed to home dampness and s. Am Rev Respirat Dis 143: Dales RE, Miller D Residential fungal contamination and health: microbial cohabitants as covariates. Environ Health Perspect 107 Suppl 3: Dales RE, Zwanenburg H, Burnett R, Franklin CA Respiratory health effects of home dampness and s among Canadian. Am J Epidemiol 134: Elidemir O, Colasurdo GN, Rossmann SN, Fan LL Isolation of Stachybotrys from the lung of a child with pulmonary hemosiderosis. Pediatrics 104: Etzel RA, Montana E, et al Acute pulmonary hemorrhage in infants associated with exposure to stachybotrys atra and other fungi. Arch Pediatr Adolesc Med 152:

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