Human leptospirosis in Queensland is associated with strong seasonal variation in incidence (Fig. 5), and risk factors for infection include male gender (Fig. 2), occupational exposure, and recreational exposure (Table 1). These results corroborate findings from many epidemiological studies of leptospirosis around the world. Variation in serovar distribution between age groups (Fig. 9) and occupations (Table 1) suggest that multiple risk factors and exposure pathways are at play, and differ between demographic groups.
Slack et al. reported the emergence of serovar Arborea in Queensland up to 2004 [11], and our study shows that Arborea has continued to emerge since that time, with increase in total case numbers, proportion of total infections attributed to this serovar (Figs. 3 and 4), as well as expansion of the serovar’s geographic distribution (Fig. 8).
Geospatial mapping showed that geographic distribution of both Arborea and non-Arborea cases varied across Queensland. Figure 6a shows that cases associated with serovar Arborea infection were mostly concentrated in the southeast coastal corner near Brisbane, and the area around Cairns and Innisfail in the northeast, and very few cases were reported from inland regions. Figure 6b shows that cases associated with non-Arborea serovars were predominantly diagnosed in the Cairns and Innisfail area, but cases were also found in the southeast coastal areas as well as more arid inland areas of the state. Figure 6c shows that locations of high crude incidence rates differed for Arborea and non-Arborea cases. Although there were insufficient cases to produce meaningful maps of annual incidence rates by cartogram regions, visual inspection shows no dramatic changes in the incidence or geographic distribution of non-Arborea serovars over the study period (Fig. 7). On the other hand, Fig. 8 shows that since its initial detection in southeast Queensland in 2001, serovar Arborea has gradually increased in both case numbers and geographic range.
The reasons for the recent emergence of serovar Arborea are currently unknown, but differences in risk between age groups, occupations, geographic location, and annual variation in incidence of Arborea versus non-Arborea serovars suggest that both behavioural and environmental factors play important roles in disease transmission. Possible environmental drivers of the emergence of serovar Arborea in Queensland over the past decade include population growth, agricultural intensification and associated deforestation, alterations in land use, and changing climatic patterns and extreme weather events. Both the Brisbane and Cairns/Innisfail areas are relatively densely populated compared to other parts of Queensland, and are surrounded by areas of intense agriculture and farming. Urbanisation is also invariably associated with the proliferation of rodents, which have been found to be carriers of serovar Arborea in Australia [20]. Globally, environmental degradation, biodiversity loss, and ecosystem stress have been linked to the emergence of infectious diseases [29], and these factors could all potentially have played a role in the recent emergence of serovar Arborea in Queensland. Considering that there are molecular similarities between Australian and European isolates of serovar Arborea, and that it had never been isolated in Australia prior to 1998, the serovar may have been introduced in recent years from international cargo ships [20], but there is no evidence to support this hypothesis.
The strong seasonal variation in incidence (Fig. 5) suggests that climate (including rainfall, flooding, and temperature) is an important driver of leptospirosis transmission in Queensland. In 2010/2011, Australia experienced one of the strongest La Nina events and wettest summers on record. From September 2010 to March 2011, the country received double its average rainfall, which resulted in widespread severe flooding and destruction of both urban and natural environments [30]. In addition, Category 5 Cyclone Yasi made landfall near Cairns in northern Queensland in February 2011, further exacerbating the already severe flooding and destruction. Natural disaster was declared in over 99 % of Queensland (total land area of 1.73 million km2) and the capital city of Brisbane experienced its worst flooding since 1974 [30]. The 2011 summer of natural disasters in Queensland was followed by an unprecedented number of leptospirosis infections, and the highest recorded proportion of infections (49 %) attributed to serovar Arborea (Fig. 3) [31, 32].
Globally, many leptospirosis outbreaks have been reported after flooding [2], but few have specifically examined the emergence of serovars associated with floods. Possible links between severe flooding and the emergence of a serovar include the proliferation of specific species of rodents that serve as reservoir hosts of the serovar; changes in environmental conditions (e.g. temperature, humidity, pH) that favour the survival of the serovar in water and soil; and increased contact between humans, animals, and floodwaters during the aftermath of disasters.
Our findings should be interpreted in light of the limitations of this study. Surveillance data recorded postcodes at each individual’s place of residence, but infections could have occurred at work, during travel to other parts of the state or country, or even overseas. Data on international travel were incomplete, and it is possible that some of the cases were acquired overseas. In Fig. 5, rainfall data were only shown for Brisbane and Cairns, but as seen in Fig. 6, many cases were reported from areas of Queensland that are far from either of these cities. Occupation was only recorded in 55.4 % of cases and it is possible that some of cases with ‘unknown occupation’ belonged to the occupational categories used for statistical analysis, thus weakening the strength of association (odds ratios and confidence intervals) reported. Results on demographics, occupation, and annual/monthly case numbers were aggregated for the whole state of Queensland, and more stratified data analysis might produce further insights into risk factors and disease ecology. Although census population data from 2011 were used to calculate crude incidence rates in each cartogram region over the entire study period (Fig. 6d), significant population growth has occurred over the study period. Cartogram regions do not correspond to administrative zones (Fig. 1), and accurate calculation of incidence was not possible, particularly with the small number of cases reported in some regions. Crude incidence rates were therefore only reported as quartiles rather than quantitative estimates (Fig. 6d).
Limitations of the MAT have already been noted, and as mentioned earlier, some of cases recorded as serovar Ballum could have been caused by serovar Arborea, but the small numbers involved (shown in Fig. 3) would not alter the overall findings or implications of our study. During the study period, the successful isolation of serovar Arborea from 63 cases (27 %) provides substantial evidence that the serovar is endemic in Queensland. Although 73 % of confirmed cases attributed to serovar Arborea were based on MAT alone, the absence of other serovars in the Ballum serogroup in Queensland (Additional file 2) significantly improves the MAT’s specificity for serovar Arborea. The database used in the earlier years of the study period recorded the number of confirmed cases attributed to each serovar, but did not allow accurately determination of the exact number of cases confirmed by each diagnostic test. The diagnostic test(s) performed varied between cases (depending on requests by clinicians and the time since onset of illness), some cases were confirmed by more than one diagnostic test, and isolations were not attempted in all cases. However, the proportion of cases confirmed by each diagnostic test does not change the overall findings or implications of our study.
If the environmental factors discussed above were indeed important in the emergence of serovar Arborea in Queensland, leptospirosis incidence could potentially escalate in the future with population growth, agricultural intensification, and increase in extreme weather events associated with climate change. Ongoing disease surveillance is therefore important for monitoring the evolution in incidence and geographic distribution of serovar Arborea, as well as early detection of possible emergence of other serovars. In high-risk areas, and particularly during the high-risk season, awareness of leptospirosis should be raised with the public, agricultural and tourism industries, and clinicians.
The transmission dynamics of leptospirosis are highly complex, and future research should aim to adopt an eco-epidemiological approach to explore the interactions between humans, animals, and the environment in determining overall infection risk and serovar emergence. Zoonotic diseases are responsible for the majority of emerging infectious diseases [29], and improved understanding of disease ecology would provide an evidence base to guide the development of tools to help predict the timing and triggers for outbreaks, determine hotspots based on environmental factors, identify subpopulations who are at greatest risk. Such tools will in turn help inform mitigation strategies, early warning systems, and public health interventions to reduce leptospirosis disease burden.