Mycobacterial aerosols and respiratory disease - Perspectives - mycobacteria prevalent in water content of aerosols

Emerging Infectious Diseases, July, 2003 by Joseph O. Falkinham, III

Environmental opportunistic mycobacteria, including Mycobacterium avium, M. terrae, and the new species M. immunogenum, have been implicated in outbreaks of hypersensitivity pneumonitis or respiratory problems in a wide variety of settings. One common feature of the outbreaks has been exposure to aerosols. Aerosols have been generated from metalworking fluid during machining and grinding operations as well as from indoor swimming pools, hot tubs, and water-damaged buildings. Environmental opportunistic mycobacteria are present in drinking water, resistant to disinfection, able to provoke inflammatory reactions, and readily aerosolized. In all outbreaks, the water sources of the aerosols were disinfected. Disinfection may select for the predominance and growth of mycobacteria. Therefore, mycobacteria may be responsible, in part, for many outbreaks of hypersensitivity pneumonitis and other respiratory problems in the workplace and home.

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Hypersensitivity pneumonitis is an occupational hazard of workers in two different industries, automobile manufacturing (e.g., metal working) and leisure (e.g., indoor swimming pools). Pulmonary illness and infection have also been a consequence of exposure to aerosols generated by hot tubs, spas, and coolant baths. Respiratory problems have also been associated with exposure to water-damaged buildings during reconstruction, and mycobacteria isolated from materials from such buildings have been shown to provoke inflammatory reactions. The outbreaks share the common feature of aerosol exposure and respiratory illness. I propose that exposure to aerosols containing mycobacteria is a common feature of the outbreaks and that mycobacteria or their products could be responsible for the respiratory symptoms.

Epidemiologic studies have established that the workers in such outbreaks were exposed to aerosols generated in the workplace from water that was either a work tool (e.g., metalworking fluid) or an integral part of the workplace or household (e.g., swimming pools and hot tubs) (1-7). Outbreaks of respiratory disease occurred in spite of disinfectant treatment of the waters or fluids to reduce the number of microorganisms. Living or working in water-damaged buildings or as a consequence of reconstruction of water-damaged buildings has also been associated with outbreaks of respiratory problems (8,9). Respiratory disease has been associated with mycobacteria in reservoirs, aerosols, or structural material in a number of cases (2,3,6,7,9).

Hypersensitivity Pneumonitis in Workers Exposed to Metalworking Fluid

An estimated 1.2 million workers in the United States are exposed to aerosols generated by metal grinding (10). Metalworking fluids are widely used in a variety of common industrial metal-grinding operations to lubricate and cool the tool and the working surface. Metalworking fluids are oil-water emulsions that contain paraffins, pine oils, polycyclic aromatic hydrocarbons, and heavy metals (10,11). Exposure to metalworking fluid aerosols can lead to hypersensitivity pneumonitis and chronic obstructive pulmonary disease (1,6,12-14). Mycobacteria were recovered significantly more frequently from metalworking fluid samples collected from facilities where hypersensitivity pneumonitis was found: compared to facilities that did not have hypersensitivity pneumonitis (6). In one study, exposure to metalworking fluid mist resulted in hypersensitivity pneumonitis in 10 workers (7). Acid-fast microorganisms identified as mycobacteria were present in the reservoir at [10.sup.7] CFU/mL (7). A mycobacteria in the reservoir was considered to be a likely cause of the hypersensitivity pneumonitis because one patient was infected by a Mycobacterium sp. and had antibodies against the reservoir fluid (7).

Hypersensitivity pneumonitis appeared in spite of disinfection of the metalworking fluid with morpholine, formaldehyde, or quaternary ammonium-based disinfectants (1,6,12,13), and mycobacteria were recovered from the metal working fluid (6,14,15). Mycobacteria are resistant to formaldehyde and quaternary ammonium disinfectants (16) and the heavy metals in metalworking fluids (17). Further, mycobacteria can grow on the organic compounds in metalworking fluid, including the paraffins, pine oils, and polycyclic aromatic hydrocarbons (18,19) and can degrade the disinfectant morpholine (20). Mycobacteria present in the water (21) can likely grow on the organic compounds in metalworking fluids in the absence of competitors after disinfection. Cleaning would not be expected to eradicate mycobacteria because of their ability to form biofilms (21,22). Adding disinfectant and cleaning the reservoir in one facility did not prevent the reappearance of mycobacteria (7 x [10.sup.5] CFU/mL by 2 weeks [7]). Further, disinfectant treatment would likely result in selection of mycobacteria remaining after the cleaning.

Hypersensitivity Pneumonitis in Swimming Pool Attendants

Granulomatous pneumonitis has been reported in lifeguards ("lifeguard lung") who worked at an indoor swimming pool that featured waterfalls and sprays (5). Affected lifeguards with symptoms worked longer hours than unaffected lifeguards (5), which demonstrated a dose-response effect. The waterfalls and sprays increased the number of respirable particles fivefold and the levels of endotoxin eightfold (5). Based on the presence of endotoxin in the aerosol samples, endotoxin exposure was suggested as the cause of the pneumonitis in lifeguards (5). However, subsequent data provided evidence of a possible second factor resulting in hypersensitivity pneumonitis; aerosols containing mycobacteria were shown to cause granulomatous lung disease (4). Others have reported high numbers of mycobacteria in swimming pools and whirlpools (23) and in hot tubs (23,24). Further, amoebae were reported in the indoor swimming pool where lifeguards reported pneumonitis (5). Mycobacteria, including M. avium and M. intracellulare, can survive and grow in phagocytic amoebae (25) and protozoa (26). In fact, M. avium grown in amoebae or protozoa are more virulent (25; Falkinham JO, unpub, data). Mycobacteria are resistant to chlorine (27) and preferentially aerosolized from water (28).