Recreational exposure to freshwater cyanobacteria : epidemiology, dermal toxicity and biological activity of cyanobacterial lipopolysaccharides

Stewart, Ian (2005). Recreational exposure to freshwater cyanobacteria : epidemiology, dermal toxicity and biological activity of cyanobacterial lipopolysaccharides PhD Thesis, School of Population Health, The University of Queensland.

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Author Stewart, Ian
Thesis Title Recreational exposure to freshwater cyanobacteria : epidemiology, dermal toxicity and biological activity of cyanobacterial lipopolysaccharides
School, Centre or Institute School of Population Health
Institution The University of Queensland
Publication date 2005
Thesis type PhD Thesis
Open Access Status Other
Supervisor Dr Glen Shaw
Dr Penny M. Webb
Prof Philip J. Schluter
Total pages 417
Language eng
Subjects 321201 Environmental and Occupational Health and Safety
321299 Public Health and Health Services not elsewhere classified
730210 Environmental health
Formatted abstract

Cyanobacteria are common inhabitants of freshwater lakes and reservoirs throughout the world. Under favourable conditions, certain cyanobacteria can dominate the phytoplankton within a waterbody and form nuisance blooms. Case reports and anecdotal references dating from 1949 describe a range of illnesses associated with recreational exposure to cyanobacteria: hay fever-like symptoms, pruritic skin rashes and gastro-intestinal symptoms (the latter probably related to ingestion of water) are most frequently reported. Some papers give convincing descriptions of allergic responses to cyanobacteria; others describe more serious acute illnesses, with symptoms such as severe headache, pneumonia, fever, myalgia, vertigo and blistering in the mouth. A U.S. coroner recently found that a teenage boy died as a result of accidentally ingesting a neurotoxic cyanotoxin from a golf course pond; this is the first recorded human fatality attributed to recreational exposure to cyanobacteria. One of the main public health concerns with exposure to freshwater cyanobacteria relates to the understanding that some blooms produce toxins that specifically affect the liver or the central nervous system. The route of exposure for these toxins is oral, from accidental or deliberate ingestion of recreational water, and possibly by inhalation Cyanobacterial lipopolysaccharides (LPS) are also reported to be putative cutaneous, gastrointestinal, respiratory and pyrogenic toxins. 

The aims of this project were to enhance the understanding of public health issues relating to recreational exposure to cyanobacteria by conducting epidemiological and laboratory-based toxicology studies. 

A prospective cohort study of 1,331 recreational water users was conducted at various sites in southern Queensland, the Myall Lakes area of New South Wales, and central Florida. The study design sought to make improvements over previously published epidemiological studies, in that an unexposed group was recruited from cyanobacteria-free waters, cyanobacterial toxins were measured in site water samples, and respondents were asked to rate the severity of reported symptoms. This study has shown an increased likelihood of symptom reporting amongst bathers exposed to high cyanobacterial cell density (measured by total cell surface area) compared to those exposed to low cyanobacteria-affected waters. Mild respiratory symptoms appear to be the predominant symptom category. 

A clinical dermatology study to examine delayed-contact hypersensitivity reactions to cyanobacterial extracts was conducted. The study groups were 20 patients presenting for diagnostic skin patch testing at the Royal Brisbane Hospital's dermatology outpatient clinic; a convenience sample of 20 individuals was recruited from outside the hospital as a control group. One patient developed unequivocal reactions to several cyanobacteria extracts, with no dose-response pattern seen, indicating that the reactions were allergic in nature. 

A mouse model of delayed-contact hypersensitivity, the mouse ear swelling test, has demonstrated that the purified toxin cylindrospermopsin, a highly water-soluble compound, is capable of producing cutaneous injury. Pronounced exfoliative lesions were seen on abdominal skin during the induction phase of these experiments. Delayed-contact hypersensitivity reactions were also demonstrated with this toxin. 

LPS from two non-axenic cyanobacterial samples - Cylindrospermopsis raciborskii and Microcystis aeruginosa - were extracted and purified Thermoregulation studies were performed using a mouse model of rectal temperature measurement. Separate groups of mice were injected with these LPS extracts at two dose levels. Thermoregulation studies were also conducted with purified cyanobacterial toxins: microcystin-LR and cylindrospermopsin and anatoxin-a; cyanobacterial LPS samples purified by collaborators in Adelaide were also investigated for thermoregulation potential. These experiments have shown that the LPS extracts are weakly active when compared with responses to much lower doses of Escherichia coli LPS. Cylindrospermopsin also produces hypothermic responses in mice - comparable to pyrexia in larger mammals - although at a later stage than was seen with LPS extracts. 

Supplementing the experimental observations of the toxicology and immunotoxicology of cyanobacterial LPS are insights gained from beyond the cyanobacteria literature on the mechanisms of toxicity of different LPS structures. Cyanobacterial LPS was initially suggested to be toxic in the 1970s, at a time when lipid A, the active moiety of LPS, was thought to be identical across all Gram-negative bacteria. More recent work raises questions about the attribution of cutaneous and gastrointestinal illness to cyanobacterial LPS, with the understanding that some bacterial lipid A structures are LPS antagonists, LPS is not toxic by the oral route, and LPS is not reported as a toxin in the clinical dermatology literature. Gut-derived lipopolysaccharides, however, exert potent synergistic effects with a variety of xenobiotic hepatotoxins, and the well-known shock-like syndromes associated with severe cylindrospermopsin and microcystin poisoning deserve further scrutiny from the perspective of immunotoxicology. 

Keyword Cyanobacteria -- Toxicology
Cyanobacteria -- Health aspects

Document type: Thesis
Collection: UQ Theses (RHD) - Open Access
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Created: Tue, 05 Apr 2005, 10:00:00 EST by Ian Stewart on behalf of Research Management Office