Endemic Melioidosis in Residents of Desert Region after Atypically Intense Rainfall in Central Australia, 2011

After heavy rains and flooding during early 2011 in the normally arid interior of Australia, melioidosis was diagnosed in 6 persons over a 4-month period. Although the precise global distribution of the causal bacterium Burkholderia pseudomallei remains to be determined, this organism can clearly survive in harsh and even desert environments outside the wet tropics.


M elioidosis, a tropical disease caused by the bacterium
Burkholderia pseudomallei, is endemic to Southeast Asia and northern Australia and is being increasingly recognized in other locations globally (1,2). During 1989-2009, a total of 540 cases of melioidosis were documented in a prospective melioidosis study based at Royal Darwin Hospital (latitude 12.4°S) in the tropical north of the Northern Territory of Australia (3). During that 20-year period, 4 of the study participants were considered to have been infected in the central Australia region of the Northern Territory; the other 536 were infected in the tropical north. During the same period, 2 persons who were not included in that study tested positive for B. pseudomallei in the central Australian region and were treated at Alice Springs Hospital (23.8°S), making a total of 6 cases of melioidosis during 20 years attributed to B. pseudomallei infection acquired in Central Australia. The ongoing Darwin prospective melioidosis study is approved by the Human Research Ethics Committee of the Northern Territory Department of Health and Menzies School of Health Research (approval 02/38).

The Study
Central Australia (also known as the "Red Centre") is the most inland part of the arid interior of Australia and features low average annual rainfall, a desert environment, and rivers that are often dry. During March-July 2011, a total 6 cases of melioidosis were diagnosed in patients from Central Australia who resided south of latitude 20°S (Figure) and had not traveled to the tropical north of the country or to overseas regions to which melioidosis is endemic. These cases occurred after exceptionally heavy rainfall in The 6 persons whose illnesses were diagnosed as endemic melioidosis were treated at the central Australia hospitals in Alice Springs and Tennant Creek (Table). Of the 6 patients, 3 were male and 5 were indigenous Aboriginal Australians; 3 became bacteremic and required intubation and ventilation in intensive care for severe sepsis. The only patient <50 years of age and no identified risk factor had the mildest disease, characterized by a localized skin abscess. All patients were treated according to standard guidelines (1): with initial intravenous ceftazidime or meropenem, then with oral eradication therapy, which is usually with trimethoprim/sulfamethoxazole. All 6 patients survived.
Rainfall in the region returned to normal patterns and there have been no further locally acquired cases of melioidosis in Central Australia. Two persons with confirmed melioidosis were treated at Alice Springs Hospital in August 2011 and December 2014; both were attributed to infection acquired while traveling to the tropical north of the Northern Territory.

Endemic Melioidosis in Residents of Desert Region after Atypically Intense Rainfall in Central Australia, 2011
B. pseudomallei isolates from the 6 patients were subjected to multilocus sequence typing (MLST) as described by Godoy et al (4). On interrogation of the global B. pseudomallei MLST database (http://bpseudomallei.mlst.net/), each of the 6 isolates was unique and a novel sequence type (ST) (Table). ST907 has 2 novel alleles (gmhD, 54 and lipA, 48) and ST905 has 1 novel allele (lepA, 44); the remaining 4 STs contained unique configurations of existing alleles. None of the 6 STs was a single-locus variant of any ST in the MLST database (i.e., sharing 6/7 alleles), but all in the database except ST904 had double locus variants (i.e., sharing 5/7 alleles) that were B. pseudomallei isolates from northern Australia. Subsequent environmental soil sampling from Central Australia has confirmed the endemic presence of B. pseudomallei in several locations, and further studies are planned to characterize the environmental correlates of such B. pseudomallei-positive sites in Central Australia (M. Mayo, B.J. Currie, unpub. data).
Historically, melioidosis has been found to occur in the wet tropics between latitudes 20°S and 20°N (5,6). Nevertheless, the first recognition of melioidosis in Australia was in an outbreak among sheep in 1949 at Winton, Queensland (22.4°S) (7), an arid location with geographic similarities to Central Australia and where flooding also sporadically occurs. Case clusters of melioidosis have also occurred even further south in Australia: 1 cluster spanned 25 years in temperate southwestern Western Australia (31°S) (8). Severe weather events with heavy rainfall have dramatically increased the case numbers in regions in Australia and overseas to which the organism is endemic (9,10) and have also unmasked melioidosis in locations where it was uncommon or not previously recognized as being endemic (11)(12)(13).
Although genotype profiles showed the 6 isolates to be closer to STs of other Australian B. pseudomallei than to STs from Southeast Asia and the rest of the world, the extensive diversity among B. pseudomallei in Central Australia is evident in that each isolate is a novel ST and that none has any known single-locus variants. This diversity is similar to the situation seen in tropical northern Australia and in northeast Thailand (14) and contrasts with endemic melioidosis identified in Puerto Rico, which was recently shown to be mostly restricted to a single ST (15). The limited genetic diversity of B. pseudomallei seen in Puerto Rico to date is consistent with more recent introduction of B. pseudomallei to that location, potentially through importation of infected animals, as has occurred elsewhere (2). Importation of infected animals from the tropical north of Australia was also considered a possible source of the clonal cluster of melioidosis seen in various animals and in a person in southwestern Western Australia (8).
Although the presence of B. pseudomallei in central Australia is clearly not a recent phenomenon, the origins and longevity of B. pseudomallei in the region and the phylogenetic relationships to B. pseudomallei in tropical Australia and elsewhere globally require further studies using whole genome sequencing. Furthermore, the geographic boundaries of B. pseudomallei across the vast interior of the Australian continent and the extent of incursion into southern Australia remain entirely unclear.

Conclusions
Heavy rains and flooding in the normally arid interior of Australia early in 2011 were followed by 6 cases of melioidosis over a 4-month period. Although the true extent of the environmental presence of B. pseudomallei remains to be determined, both regionally and globally (1,2), these bacteria can clearly survive in harsh and even desert environments outside the traditionally recognized melioidosis-endemic regions of the wet tropics. Melioidosis should therefore be considered in such regions, especially after heavy rainfall and flooding.