Scrub typhus, a major febrile disease, is prevalent in Asian countries, including China, Japan, and Korea [1,2]. Orientia tsutsugamushi, the causative agent of scrub typhus, is transmitted to humans through the bite of infected trombiculid mites [3, 4]. Apodemus agrarius is a dominant wild rodent that harbors infected chigger mites [5]. Forty-four species of chigger mites, including L. pallidum, L. scutellare, L. palpale, L. orientale, and L. zetum, have been reported as vectors of scrub typhus in Korea [6]. The chigger indices and seropositive rates of scrub typhus in wild rodents were highest in autumn. Because trombiculid mites lay eggs in the summer in Korea, the incidence of scrub typhus in humans peaks in the autumn months [3,7–9]. The annual number of scrub typhus cases had increased to 10,365 in 2013.

Several epidemiological data on the abundance of chigger mites, their hosts, and geographic distribution have been published; however, most have focused on limited areas. In this study, we investigated the nationwide geographical distribution of chigger mites (Leptotrombidium species) in striped field mice (A. agrarius) in Korea during the scrub typhus outbreak season (October and November). In addition, we analyzed the relationship between chigger mites and weather conditions and the incidence of scrub typhus.

A total of 233 A. agrarius were captured at 16 study sites for 3 years. The yearly trapping rates were 12.2%, 12.5%, and 12.0% in 2009, 2012, and 2013, respectively. All adult A. agrarius were infested with chigger mites (Table 1). The yearly average chigger indices of Leptotrombidium species from A. agrarius are shown in Table 2. The chigger index was highest in Chungcheongbuk-do (358.3) followed by Jeollabuk-do (305.4) in 2009, Chungcheongbuk-do (290.1) followed by Chungcheongnam-do (286.2) in 2012, and Chungcheongnam-do (294.4) followed by Chungcheongbuk-do (240.0) in 2013. There was no significant difference in the chigger indices among the years. The predominant chigger mites were L. pallidum and L. scutellare. The average chigger index of L. pallidum at each site ranged from 0 to 294.6, and that of L. scutellare ranged from 0 to 210.0. L. pallidum was predominant at 13 collection sites (Goseong, Sokcho, Hwacheon, Taebaek, Paju, Hwaseong, Asan, Buyeo, Cheongju, Gunsan, Gimje, Gimcheon, and Yeongdeok), and L. scutellare at 3 collection sites (Gimhae, Gwangyang, and Boseong) (Fig. 2). L. palpale, L. orientale, and L. zetum showed uneven geographical distributions and very low chigger indices (0–12.5). The chigger index of L. pallidum was negatively correlated with temperature (P=0.036) and positively correlated with relative humidity (P=0.022). Meanwhile, the chigger index of L. scutellare was positively correlated with temperature but not significant (P=0.200). The chigger index was not affected by precipitation (Fig. 3). Moreover, the chigger index of L. scutellare was positively correlated with the prevalence rate of scrub typhus (Fig. 4).

In this study, all adult A. agrarius were infested with chigger mites. It is known that the chigger infestation rate was variable. It was dependent on the seasons, and was highest during autumn and lowest during summer in Korea [3,11,12]. L. scutellare was not found in 5 collection sites (Goseong, Sokcho, Hwacheon, Taebaek, and Paju) located in the northern and eastern parts of Korea, whereas L. pallidum was not found in 3 collection sites (Gimhae, Gwangyang, and Boseong) located in the southern parts of Korea (Fig. 2). The geographical distribution of L. scutellare varied by collection sites. It was found in the southern and western areas, but not in the northern areas, Korea [3,8]. It is reported that L. scutellare is found in areas where the annual average air temperature is >10°C [13]. A previous study in October and November 2006 showed that A. agrarius in Chungcheongbuk-do, Chungcheongnam-do, Gyeonggi-do, and Gangwon-do was not infested with L. scutellare [8], while in this study, L. scutellare was found in Chungcheongbuk-do, Chungcheongnam-do, and southern area of Gyeonggi-do (Hwaseong). Chigger index of L. scutellare decreased in the northern and eastern areas of Korea. Recent reports have shown that L. scutellare was also found in Hwaseong in October and November 2015, and the ratio of L. scutellare to L. pallidum was increased to 0.58 [14]. In this study, the average ratio of L. scutellare to L. pallidum in Hwaseong for 3 years (2009, 2012, and 2013) was 0.05. L. pallidum was found in southern provinces, such as Jeollanam-do and Gyeongsangnam-do but not Jeju-do in 2005, 2006, and 2007 [3,8,15]. In this study, L. pallidum was not found in Jeollanam-do and Gyeongsangnam-do in 2009, 2012, and 2013. Taken together, these data strongly suggest geographical distribution of L. pallidum and L. scutellare was changed. The chigger index increased after hot and humid summers [16] and moist soil was suitable for chigger survival [9]. A possible explanation is that global warming might affect the distribution and trigger indices of L. pallidum and L. scutellare. In this study, precipitation had no relationship with the chigger indices of L. pallidum and L. scutellare. Precipitation is known to influence mite development, reproduction, and population dynamics [17]. Because we performed this survey during the autumn season, it is possible that there was no correlation between precipitation and the chigger index.

The chigger index of L. scutellare, but not L. pallidum, was correlated to the incidence of scrub typhus in this study areas. This is in agreement with a previous study demonstrating that the geographical distribution of the chigger index of L. scutellare was identical to the incidence of scrub typhus [15], and the relative population density of chigger mites was associated with an annual increase of scrub typhus cases in autumn [8,11]. This coincidental geographical distribution of L. scutellare and scrub typhus cases was also reported in Japan [18]. In Korea, the infection rate of O. tsutsugamushi was high in L. palpale (5.3%), followed by L. scutellare (3.7%), L. orientale (3.6%), and L. pallidum (1.5%) [19]. Although the predominant species of chigger mites in Korea were L. pallidum and L. scutellare, the infection rate of O. tsutsugamushi in L. scutellare was much higher than that in L. pallidum. The distribution and high population of L. scutellare had been expanded in the northern parts of Korea. In addition, the occurrence of scrub typhus gradually extends northward [12]. These findings also support our data that the incidence of scrub typhus is positively correlated with L. scutellare.

This nationwide epidemiologic study of chigger mites in wild rodents will provide necessary baseline data for distribution of chigger mites and for controlling scrub typhus.