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Recollections: Assessment of Tick-Borne Diseases in Hainan Province, China

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    沈阳化工大学材料科学与工程学院 沈阳 110142

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Assessment of Tick-Borne Diseases in Hainan Province, China

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Abstract

China’s six tropical regions include Guangdong Province, Yunnan Province, Hainan Province, Hong Kong Special Administrative Region (SAR), Macau SAR, and Taiwan, China. Hainan, seated in the southernmost tropical region of China, is home to ticks that remain active throughout all four seasons. This heightens their potential to transmit tick-borne diseases to both animals and humans. This study provides a succinct overview of the prevailing tick species’ spatial distribution and offers an outline of the range and dispersion of emerging tick-borne infections in tick vectors, animal hosts, and human populations within Hainan, China.

  • 1. Key Laboratory of Tropical Translational Medicine of Ministry of Education, NHC Key Laboratory of Tropical Disease Control, School of Tropical Medicine, Hainan Medical University, Haikou City, Hainan Province, China
  • Corresponding author:

    Qianfeng Xia, xiaqianfeng@hainmc.edu.cn

  • Funding: Supported by the Major Science and Technology Program of Hainan Province (grants ZDKJ202003, ZDKJ2021036, and SKJ10006). Additionally, financial support was received from the National Natural Science Foundation of China (grant 81960002) and the Science and Technology Plan of Hainan Province (specifically, the Hainan Province Clinical Medical Center, SRC220002). The research benefited from a grant awarded by the Hainan Provincial Natural Science Foundation of High-Level Talent Project (821RC1152)
  • Online Date: September 15 2023
    Issue Date: September 15 2023
    doi: 10.46234/ccdcw2023.157
    • China encompasses six tropical regions, namely Guangdong Province, Yunnan Province, Hainan Province, Hong Kong Special Administrative Region (SAR), Macau SAR, and Taiwan, China. Of these, Hainan occupies the southernmost tropical region of China, notable for active vectors year-round which enhances their capacity to transmit vector-borne diseases (VBDs) to both animals and humans (1-2). Emerging and reemerging tick-borne diseases (TBDs) play a significant role in VBDs and present new health challenges to both humans and animals on this tropical island. The first recording of ticks on Hainan Island dates to 1981 with the documentation of a novel tick species, Amblyomma hainanensis, by the distinguished Chinese acarologist Kuofan Teng (commonly known as Guofan Deng in contemporary Chinese pronunciation) (3). Further, in 1985, the initial tick-borne pathogen (TBP), indicated by seropositivity to spotted fever group Rickettsia (SFGR), was identified in six of 402 healthy volunteers from the island (4). Since then, Professor Bihu Li has been recognized for significantly contributing to the reporting and research of Rickettsia infections in Hainan (5-7). The discovery of severe fever with thrombocytopenia syndrome (SFTS) in Chinese mainland led to an increase in research on ticks and TBDs on Hainan Island. This study presents a succinct overview of the spatial distribution of tick species and illuminates patterns in the types and distribution of emerging tick-borne infections in tick vectors, animal hosts, and humans.

    • In conducting a systematic review of current citations on ticks in Hainan (methods detailed in the Supplementary Material), 21 species of hard ticks were identified. These include ten Haemaphysalis species, five Amblyomma species, three Rhipicephalus species, one Ixodes species, one Hyalomma species and one Dermacentor species. These were discovered on the island, representing approximately 17% of the 124 tick species in China (8). As of yet, there’s no record of soft ticks from Hainan Island.

      The Rhipicephalus genus is the most common tick genus found on Hainan Island, albeit consisting only of three species — Rhipicephalus sanguineus sensu lato(s. l.), Rhipicephalus haemaphysaloides, and Rhipicephalus microplus. Rhipicephalus ticks have been recorded almost everywhere on the island except for the southwestern county of Dongfang, the eastern county of Qionghai and the southeastern county of Linshui (9-17) (Figure 1).

      Figure 1. 

      Geographical distribution of hard ticks on Hainan Island in China, 1980–2023.

      Haemaphysalis formosensis, Hae. cornigera, Hae. mageshinaensis, Am. hainanense, Am. helvolum, and Hy. isaaci were not drawn on the map due to the unspecified place recorded in the references.

      Haemaphysalis ticks are plentiful in Chengmai, Qiongzhong, and Sanya City but much less common in Wanning, Haikou City, and Changjiang. They have not been recorded in the rest of the island’s counties or cities (917) (Figure 1). Amblyomma ticks have been reported in only five locations, inclusive of Chengmai, Lingao, Dingan, Qiongzhong, and Sanya (9,11,1718) (Figure 1).

      Ixodes granulatus has been documented in Haikou, Chengmai, Baisha, Qiongzhong, Wanning, and Sanya counties, with three incidences in Chengmai and Qiongzhong counties (10-17,1920). The remaining species, Dermacentor auratus and Hyalomma isaaci, have likewise been recorded (911,13,15,17,18,2122) (Figure 1). The host of these hard ticks on the island varies and ranges from birds and reptiles to mammals (Supplementary Table S1, available in https://weekly.chinadc.cn).

    • A comprehensive review of existing literature on TBPs in Hainan was undertaken (detailed methodology is provided in the Supplementary Material). The agents infecting ticks, animals, and humans can be classified into three categories: bacteria, protozoans, and viruses. Bacteria constitute the principal category of TBPs, represented by twenty species, including six Borrelia, four Anaplasma, four Rickettsia, four Ehrlichia, and two Coxiella species. Protozoans form the second largest group with ten species, including four Babesia, five Theileria, and one Hepatozoon species. There are only two known viral pathogens: a novel Alphavirus and the Crimean-Congo hemorrhagic fever virus (CCHFV). In the eighteen administrative divisions, TBPs are predominantly reported in the central and northern regions, with fewer instances cited in the southern parts of Hainan Island (Figures 25).

      Figure 2. 

      Geographic distribution of emerging infections caused by agents in the Anaplasma genus in ticks and animals in Hainan, China.

      Note: In an uncharted area of the region, infection with Anaplasma marginale was detected, expanding its known presence to Haikou, the region’s capital. Samples collected from Baisha, Ledong, Dingan, and Tunchang tested positive for A. platys with an infection rate of 1.1%. For the purposes of this study, specific values were assigned to each site: Baisha, Ledong, Dingan, and Tunchang.
      Figure 3. 

      Geographic distribution of emerging infections from viruses and bacteria, excluding the Anaplama genus, in ticks and animals in Hainan, China.

      Abbreviation: CCHFV=Crimean-Congo haemorrhagic fever virus.
      Figure 4. 

      Geographic distribution of emerging protozoan infections in ticks and animals in Hainan, China.

      Note: A documented case of Babesia vogeli infection was identified in an unspecified area of the region, extending its known occurrence to Haikou, the capital of this region. Furthermore, a case of Babesia bovis infection, previously found in Central Hainan, has now been registered within the location of Qiongzhong. The term “Qiongzhong” in Chinese denotes “Central part of Hainan,” accurately portraying its geographical siting in the central part of the island.
      Figure 5. 

      Documented distributions of human tick-borne pathogen infection at the county level in Hainan, China.

      Note: The documentation of infections from the spotted fever group Rickettsia, Anaplasma phagocytophilum, and Ehrlichia chaffeensis has been extended to include an unidentified region within Haikou. Similarly, a case of infection with an uncharacterized species of Borrelia in the central area of Hainan has been reported in Qiongzhong.

      Rickettsia species have emerged as the primary pathological agents causing TBDs in Hainan Island, China, with documented human infections present throughout the region. Cases have been noted in Chengmai and Haikou to the north, Qionghai and Wanning to the east, Qiongzhong in the center, Danzhou City to the west, and Sanya to the south (6,12,23-25). As of mid-2023, the identified species of Rickettsia on Hainan Island include Rickettsia siberica, Rickettsia heilongjiangiensis, and an unidentified member of the SFGR group (6,12,23-25) (Figures 2 and 5, Supplementary Tables 2–3).

      Species of Anaplasma reported in the region include Anaplasma bovis, Anaplasma marginale, Anaplasma phagocytophilum, and Anaplasma platys. Anaplasma, predominantly located in the northeastern areas of Hainan, like Haikou and Qionghai, but with instances of A. platys infections in the southwestern and southern zones (11,26-30). Reservoir hosts for A. phagocytophilum on the island may include cattle, goats, and dogs, with Rh. sanguineus and Rh. microplus reported as potential vector species for agent circulation (26,2829,31) (Figures 3 and 5, Supplementary Tables S2–S3).

      Genospecies of Borrelia burgdorferi s. l., including Borrelia garinii, which cause human Lyme borreliosis, have been detected in human cases in Haikou (23), and other uncharacterized genospecies of Bo. burgdorferi s. l. have infected individuals in Wenchang, Danzhou, Dongfang, Qiongzhong, Haikou, and Sanya, with prevalence rates between 1.99% and 9.96% (3233). Four spirochetes of the Bo. burgdorferi s. l. group, including Borrelia afzelii, Bo. garinii, Borrelia valaisiana, and Borrelia yangtzensis, were found in Rh. microplus ticks ( Figures 3 and 5, Supplementary Tables S2–S3).

      Tick-borne protozoan infections, significant threats to animal health, have been frequently reported in the northern part of Hainan Island, especially in Dingan, Haikou, Danzhou, and Chengmai (11,30,3437) (Figure 4, Supplementary Table S2). Also, two tick-borne viruses carry potential implications for bovine health; a novel Alphavirus was identified in ticks from cattle in Danzhou (38), and anti-CCHFV IgG was confirmed in bovine serum samples from Haikou, Chengmai, Dongfang, and Sanya (39).

    • The tick species Haemaphysalis longicornis is among the most extensively distributed across Chinese mainland, yet it has been identified in merely three out of 18 administrative regions on Hainan Island (8,11,17,4041). This uneven distribution may be attributed to the potential limited exploration of hosts and associated vegetation types within other regions, which may consequently introduce a bias in its perceived distribution.

      Serological methods have detected instances of human infections with SFGR on Hainan Island, an indication of the natural circulation of SFGR in this region. As such, there is a pressing need to intensify efforts to monitor infection rates and assess the risk of pathogen spillover from ticks and animals to humans in urban areas or counties where no human infection has been reported to date.

      Recent years have seen an increased involvement of scientists from diverse academic backgrounds in tick and TBD research. This has undoubtedly broadened the scope of research topics and enriched academic discourse. However, this growth also introduces potential issues concerning data reliability, particularly regarding potential misidentification errors due to minor morphological differences amongst tick species, lack of researcher expertise, or inaccurate description of new species. As an illustration, the Hae. longicornis species was often confused with Haemaphysalis bispinosa in South China until a clarification was made based on dental formula differences and distinctly pointed spurs on coxae II–IV, a morphological feature specific to Hae. bispinosa (42). Inexperienced researchers, particularly in regions where Haemaphysalis hystricis and Hae. longicornis coexist, may encounter difficulties correctly distinguishing them. However, the two species can be readily identified by noting differences in dental formula and body size: Hae. longicornis has a 5/5 dental formula and a smaller body size compared to Hae. hystricis, which possesses a 4/4 dental formula (43). To ensure data reliability, crucial in assessing tick and TBD risks, it is suggested that future researchers in tick identification collaborate with acarologists and employ molecular methods as means of verification and validation.

      Ticks have been observed to be concentrated in specific regions of Hainan, China such as Chengmai, Qiongzhong, and Sanya, but appear less common in areas like Wenchang, Baisha, and Wuzhishan. Remarkably, several regions including Qionghai, Dongfang, Baoting, and Lingshui have yet to record any tick species. However, this distribution does not align with the clustering of TBPs which predominantly occur in northern Hainan, specifically in Dingan and Haikou.

      It appears that investigations into ticks and TBPs are incomplete in several areas, evidenced by absent or inadequate reports from locales such as Dingan, Haikou, and Sanya. To rectify this, the implementation of thorough surveillance for both ticks and TBPs is strongly advised under the following conditions: 1) where surveys have not yet been undertaken; 2) where ticks and TBPs are pervasive and surrounding areas have reported none or minimal occurrences; 3) where TBPs are rife, though ticks are sparsely identified; 4) where tick sightings are frequent, necessitating intensive TBP detection; 5) where ticks and TBPs demonstrate high infection rates in humans and animals, necessitating strict monitoring of TBDs; and 6) if TBDs become epidemic, causing significant morbidity or mortality, and existing in similar latitudinal, biogeographical, or microclimatic conditions.

      Finally, to streamline and boost the effectiveness of these efforts, the establishment of a comprehensive surveillance system for ticks and TBDs is critical.

      The present study exhibits certain limitations. Initially, the non-random nature of the chosen locations for surveying ticks and TBPs could have potentially introduced bias into the determination of the distribution of ticks and TBPs. Furthermore, the majority of the ticks and TBPs were extracted from domestic animals, raising the likelihood of excluding ticks and TBPs associated with wild animals within the surveyed locations. Moreover, some ticks and TBP detection records used in the study date back more than four decades; given this substantial period, significant changes should be anticipated in the habits of ticks and TBPs. Despite these constraints, the study still offers valuable insights into understanding ticks and TBDs in Hainan, China.

    • Professor Guojing Yang and Mr. Mingfa Li for illustrating the geographical distributions of ticks and TBPs.

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