Temporal Association of Meteorological Parameters and Scrub Typhus Incidence, and Relationship between Ectoparasitic Mite and Small Mammal Orientia tsutsugamushi Infection Status, in Western Yunnan Province, China

Abstract

BackgroundScrub typhus is an important public health concern in China. Small mammals and their parasitic mites can serve as proxy indicators, with their abundance and Orientia tsutsugamushi (Ot)infection patterns can provide early warnings signals for humans. Environmental factors, such as meteorological parameters, land cover and vegetation, etc., are also crucial in scrub typhus transmission; influencing the abundance of hosts and vectors as well as human activities. However, there remains a lack of comprehensive studies that simultaneously explore the association between hosts, vectors, pathogens and environmental variables, especially in western Yunnan, China, where scrub typhus incidence is particularly high compared to other provinces. This highlights the need for integrated research efforts to enhance understanding of the dynamics of scrub typhus transmission in endemic areas.ObjectiveTo explore the temporal association between meteorological parameters and scrub typhus incidence, the association between the abundance of parasitic mites in host and environments, and the association of Ot infection and genotypes in two populations.MethodsFor Part 1, secondary scrub typhus cases data obtained from the Chinese National Notifiable Infectious Disease Reporting Information System in the Chinese Center for Disease Control and Prevention and meteorological parameters from the China Meteorological Data Service Center were used. Distributed lag non-linear models were applied to explore the relationship between meteorological parameters (Monthly mean-, maximum-, minimum- temperatures, temperature range, relative humidity and precipitation) and scrub typhus incidence from 2010 to 2019 in Baoshan City, western Yunnan Province. The relative risks and 95% confidence interval at different exposure level and lag months were estimated.For Part 2, a cross-sectional study was conducted and data were collected in July 2022 in Tengchong City, western Yunnan Province. Three landscapes and four locations were selected as the sampling sites to capture small mammal and collect ectoparasitic mites. Subsites were designed in per landscape of each location. The hurdle negative binomial (HNB) mixed model was employed to analyzed the association between host and vector and environment, subsites was set as random element. The probability of infestation prevalence odds ratios (OR) and intensity ratios (IR) were calculated. Ot infection of small mammals and parasitic mites were detected in Nested polymerase chain reaction (NPCR) and identified in phylogenetic analysis.ResultsFor Part 1, high monthly mean (20°C) and maximum (30°C) temperatures were associated with a peak risk of scrub typhus in the current month (lag=0 month). Higher minimum temperatures and higher relative humidity were followed by increasing cumulative risks over the ensuing 3 months. Higher precipitation was followed by increasing cumulative risk over the ensuing 2-month period, peaking at around 30cm. Considering the predicted overall cumulative risk of scrub typhus over the ensuing 4-month period (0 to 3 month lags), the risk peaked following a moderate-to-low mean and maximum temperatures, (14°C and 23°C, respectively, around the 25th percentile level), high minimum temperature (16°C, around the 75th percentile), and moderate to high precipitation (10cm, around the 75th percentile), though possibly also peaking following particularly high precipitation levels of around 30cm. Increasing cumulative risk was seen for relative humidity increasingly above median levels (70%).For Part 2, a total of 321 small mammals with 24 diverse species captured in Tengchong City, Rattus tanezumi, Suncus murinus, Rattus rattus and Mus pahari were the dominant species. Ninety-seven mammals were infested with mites, giving an overall infestation prevalence of 30.2%; 9562 mites were collected, and the mean mite abundance and mite intensity were 29.79 mite per small mammal and 98.58 mite per infested small mammal, respectively. Only one sample of small mammals was detected positive for Ot, with Karp strain based on the 56 kDa gene. For the effects of the occurrence of mites in small mam mals by location and landscape, the infestation prevalence among small mammals was the highest in the southern forest; moreover, the southern, eastern and western farmland and eastern forests also had a significantly higher prevalence odds than in the combined residential areas (P<0.05). Compared to non-dominant species in each specific location, Rattus nitidus and Mus pahari had significantly higher mite intensities in north location; Rattus rattus and Rattus tanezumi had a significantly higher probability to be infested with mites in east location; Neotetracus sinensis had a significant higher probability and mite intensity in west location. Rattus rattus, Rattus tanezumi and Crocidura dracula showed a significantly higher probability to be infested with mites in the south location; however, only Rattus rattus had a significant higher mite intensity. Infestation prevalence was significantly lower in the forest in the west location and in the residential area in the south compared to farmland in the respective locations. Conclusion The non-linear lag associations between meteorological parameters and scrub typhus incidence suggest that higher monthly minimum temperature and relative humidity could be associated with an increased risk of scrub typhus in the subsequent several months, while warm temperature is more likely to impact the occurrence of scrub typhus in the current month. Diverse small mammals were captured in Tengchong City. Rattus tanezumi, Suncus murinus, Rattus rattus and Mus pahari were the dominant species. Rattus rattus had the highest infestation prevalence and Neotetracus sinensis had the far highest mite intensity. The HNB mixed effect analysis showed landscape and location of capture significantly influenced infestation prevalence and mite intensity in small mammals. Specifically, dominant species in specific locations demonstrated a significantly higher infestation prevalence in the east, west, and south locations, while mite intensity was significantly higher in the north, west, and south locations. Notably, small mammals captured in the residential area of the south and in the forests of the west had significantly lower infestation prevalence.