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Dangerous Ground

Tim Inglis searching for B. pseudomallei in the Kimberley.

Tim Inglis searching for B. pseudomallei in the Kimberley.

By Tim Inglis

A deadly bacterium lies dormant in tropical soils until it is disturbed by natural disasters, mining operations or even gardening.

Outbreaks of serious infectious diseases were predicted after the first wave of floods in Pakistan. Weeks later those predictions were proved sadly accurate as the human tragedy unfolded, with further flooding adding to the human misery caused by cholera, malaria, dengue and skin infections.

The scale of this disaster dwarfed the Indian Ocean tsunami that occurred on Boxing Day in 2004. In both of these events a short list of infectious diseases appeared high on the list of priorities for medical relief workers preparing to join the international aid effort. Dominating the headlines was cholera, a disease feared even more than typhoid and dysentery, probably due to its ability to spread so quickly. These and other gastrointestinal infections are a common result of the toxic combination of a natural disaster, a large number of displaced people and a lack of basic sanitation.

But you can guarantee that one potentially fatal tropical infection, known as melioidosis, will not even appear on the radar until after long after the onset of disaster. This soil-borne infection was diagnosed in a series of sporadic cases in the wake of the 2004 tsunami at points around the Indian Ocean. As it can be remarkably difficult to diagnose, we can predict that the majority of melioidosis cases in flood-ravaged Pakistan will go undetected.

Warm and Wet
In Australia, melioidosis is an infection of warm, wet places across the north of the continent. Cases of severe infection, normally accompanied by bacteria in the bloodstream, peak during the wet season days to weeks after the onset of the first rains.

In northern Australia there will be around 50–100 acute cases confirmed each year, the largest proportion usually coming from the Northern Territory. Around 15–20% these cases will die, even with expert medical treatment.

Cases are more frequent in years with higher summer rainfall, particularly when severe weather events such as cyclones or tropical storms occur. The reasons are not clear, but we believe it is more than just a matter of adding water.

What we do know is that the bacterial cause of melioidosis, Burkholderia pseudomallei, can survive in the environment for a very long time. Experiments have shown that this tough bacterial species can persist for years in distilled water, so it is possible that these bacteria persist in deeper layers of soil that stay moist even during the long dry season.

However, research suggests there may be a bit more to it than that. We have shown that these bacteria can burrow into free-living amoebae and fungi that live in the soil, then stay there for long periods without seriously damaging their host. We have suggested that sheltering inside these more larger soil organisms could be crucial to the long-term survival by B. pseudomallei in tropical soils.

Another possible explanation for the peak risk of melioidosis in the wet season may be the vulnerability of these bacteria to ultraviolet light. They may be tough in some ways, but do not survive exposure to the midday sun in Perth. We suggest that a loss of the sterilising effect of ultraviolet light during the wet season in northern Australia could partly explain the seasonal pattern of human infection.

Not Just Wet but Windy Too
Recent surveillance data on melioidosis in the Northern Territory shows how cases of severe melioidosis peak when cyclones blow through. Western Australia has some of the most cyclone-ravaged coastline in the Southern Hemisphere. Shortly after melioidosis became a notifiable infection in WA, we became storm-watchers and noticed with great interest how the area we consider to be the endemic zone for melioidosis in WA is gradually extending each time a cyclone travels inland in a southwesterly direction. The latest addition to the WA melioidosis map includes communities as far from the ocean as Wiluna, which is approximately 800 km inland.

By happy coincidence we were collecting environmental and workforce blood samples on a large mine site in the East Kimberley when a small tropical storm blew through, bringing an all-time record rainfall and strong winds at the same time. By comparing blood tests before and after the storm we could show that there was an increase in exposure to Burkholderia. Environmental samples collected after this unusually severe weather event led to the detection of the same strain of B. pseudomallei that caused an outbreak 500 km to the west 8 years before.

As this particular strain has not been seen in human infections or environmental samples in the intervening period, it is probable that the outbreak strain of bacteria has travelled on the prevailing wind, and possibly in a tropical storm. When rainfall records from that site were checked we were able to find an increase in annual rainfall over 22 years with an interesting 5–7-year cyclical pattern, suggesting a possible connection with an El Niño effect.

Dig Deep and Spread It Wide
An incidental observation from the mine site study was that B. pseudomallei was only present in transitional environments where attempts were being made to restore native vegetation. The bacteria were absent where topsoil had been removed completely to get at rock and in places that had been kept in a pristine condition.

The places where soils are actively managed by hand in northern Australia are private gardens, so it is no coincidence that melioidosis is known in Darwin as “Nightcliff gardeners’ disease”. We have seen infection of skin and underlying tissues in people who tend their own gardens in several towns along the Great Northern Highway. Many people in Darwin know about the risks of gardening in the wet season due to annual public health warnings, but knowledge of the hazard is patchy elsewhere. It remains to be seen whether the expansion of the Ord River scheme will increase the small number of cases we see from the Kimberley each year.

Rather ominously, the first rice crop in WA for many years was announced earlier this year. In South-East Asia, rice farmers are among the occupational groups at highest risk of melioidosis, particularly in countries such as Thailand where there are many more cases of the infection each year than we see in all of northern Australia.

Health departments across the tropical north have kept a melioidosis watch for more than a decade in the case of Queensland and the Territory, and since 2000 in WA. Interstate collaboration has helped the disease-watchers to keep their eye on any possible trends so we can say with some confidence that there has been an unusually large number of cases of melioidosis this year in the Northern Territory, coinciding with heavy rains.

More subtle has been a possible edging upwards of the smaller annual number of melioidosis cases in WA. We expect that this total will increase with the expected growth of the mining and agriculture sectors in the north-west, before taking into account any consideration of exposure that comes from specific types of work. More people living in the region will mean more cases unless preventative methods become more effective.

Stopping the Rot or Stopping the Lot?
There is no vaccine for melioidosis. Attempts have been made to develop one, but have so far proved only partly successful. The difficulty is that this bacterial species can lie dormant in a patient’s cells (possibly like it does in amoebae or fungi) for very long periods, protected against the effects of the person’s immune system. A vaccine therefore has to do more than just raise antibodies. It needs to produce what is sometimes called sterilising immunity.

In the meantime we have to rely on environmental controls, beginning with the common sense approach of minimising contact with moist tropical soils during the wet season, carefully washing any skin abrasions or cuts immediately after the trauma occurs, and staying indoors during severe weather. In the case of the rare water-associated outbreaks such as the one in the Kimberley in late 1997, better disinfection of the drinking water appears to prevent cases of infection. Measures taken after that outbreak are the probable cause of an absence of any further cases in that community and surrounding settlements.

The key response we set up in early 1998 was improved chlorine treatment of drinking water supplies. We also removed an obsolete water treatment plant called an aerator that may have functioned as a bacterial amplifier prior to the outbreak. We ensured there were good seals on water supply pipelines, some of which had corroded because unusually acidic water let soil into contact with the water.

Safer Soils?
Careful study of melioidosis distribution shows a tendency for it to occur in pockets or hot spots. The reason why particular locations harbour a population of B. pseudomallei at levels that can cause human infection remains unknown.

We speculate about how people encounter this bacterial species and what factors beyond raw bacterial numbers and human vulnerability influence the probability of infection. Encounter with these bacteria does not inevitably lead to infection. In over a decade of fieldwork including exposure to live B. pseudomallei in its natural habitat on several occasions, I have yet to show any evidence of exposure.

Mention has already been made of the association between B. pseudomallei and transitional soils in our mine site study. Studies of soils from other parts of the melioidosis endemic region suggest that how we care for the land may influence the potentially pathogenic bacteria that lurk close to the surface.

Field work in Eastern Malaysia has confirmed that B. pseudomallei was absent from upland rice fields managed with organic fertiliser and single cropping. These bacteria were also absent from traditional hillside rice plantations that were downstream of locations where the infection was present in riverbank communities.

Interestingly, repeat sampling at a location east of Perth, where a lengthy outbreak of melioidosis in goats coincided with a serious loss of crop productivity, now returns consistently B. pseudomallei-free soil cultures and is infection free. That property has been replanted with native species as part of a local bioremediation program.

These observations raise more questions than answers, but give us a few clues as to how we might tackle the challenge of a potentially fatal disease caused by an environmental encounter with Burkholderia-contaminated soils.

Tim Inglis is a medical microbiologist with PathWest Laboratory Medicine WA, QEII Medical Centre, Perth.