Distribution and Ecological Drivers of Spotted Fever Group Rickettsia in Asia

Abstract

Spotted fever group and related rickettsia (SFGR) are a neglected group of pathogens that belong to the genus Rickettsia. SFGR are zoonotic and are transmitted by arthropod vectors, primarily ticks, fleas and mites to accidental hosts. These emerging and re-emerging infections are widely distributed throughout the world. Land-use change and increasing human–wildlife conflict compound the risk of SFGR infection to local people in endemic areas and travelers to these regions. In this article, we discuss the rickettsial organisms causing spotted fever and related diseases, their arthropod vectors in Asia and the impact of land-use change on their spread.

Introduction

Rickettsioses are infectious diseases caused by obligate intracellular gram-negative bacteria. They belong to the order of Rickettsiales, family Rickettsiaceae (Fournier and Raoult 2009) and reside in a wide range of arthropod vectors such as fleas, ticks and mites (Chikeka and Dumler 2015; Merhej et al. 2014). These vectors can transmit pathogens to humans at the bite site, who may or may not subsequently develop disease. Rickettsial diseases have been reported to be the second most common cause of non-malarial febrile illness in the Southeast Asia region after dengue infection (Acestor et al. 2012).

The family Rickettsiaceae comprises Rickettsia and Orientia genera as members and is divided into three major groups; spotted fever group (SFGR), typhus group (TG) and scrub typhus group (STG) (Bhengsri et al. 2016). Rickettsial diseases have worldwide distribution although there are endemic and hyper-endemic areas (Chikeka and Dumler 2015; Luce-Fedrow et al. 2015; Merhej et al. 2014). Typhus group and scrub typhus group are widely diagnosed in Southeast Asia (Aung et al. 2014; Parola et al. 2013; Rodkvamtook et al. 2013). In Asia, typhus group infections are primarily caused by Rickettsia typhi which is the etiologic agent of murine typhus (endemic typhus) with a few cases of epidemic or louse-borne typhus caused by R. prowazekii reported. Scrub typhus is widespread in Asia–Pacific and northern Australia and is caused by Orientia tsutsugamushi along with the related O. chuto (Chikeka and Dumler 2015; Izzard et al. 2010).

SFGR consists of at least 30 species that can be found worldwide. Twenty-one species are identified as pathogens: R. rickettsii, R. parkeri, R. africae, R. massiliae, R. philipii, R. conorii, R. sibirica, R. slovaca, R. raoultii, R. monacensis, R. aeschlimannii, R. helvetica, R. heilongjiangensis, R. japonica, R. honei, R. tamurae, Candidatus Rickettsia kellyi, R. australis, R. mongolotimonae, R. felis and R. akari. Nine species are of unknown pathogenicity: Candidatus Rickettsia asemboensis, R. bellii, R. montanensis, R. peacockii, R. rhipicephali, R. monteiroi, R. gravesii, and R. argasii (Fournier and Raoult 2009; Merhej et al. 2014). There remains some conjecture as to the status of R. felis and R. akari within SFGR (Chikeka and Dumler 2015). There is an argument that R. felis and R. akari should be reclassified into a transitional group (Gillespie et al. 2008) on the basis of phylogenetic analysis, however, at this point in time they remain classified as members of the SFGR (Fournier and Raoult 2009; Merhej et al. 2014; Vitorino et al. 2007).

The most well-known rickettsia is R. rickettsii which causes Rocky Mountain Spotted Fever (RMSF) and causes human infections predominantly in the USA (Kato et al. 2013). Other species such as R. australis and R. honei are prevalent in northern Australia (Graves and Stenos 2009). Rickettsia conorii is responsible for Mediterranean Spotted Fever (MSF) in several parts of Europe, Africa and Asia (Nanayakkara et al. 2013; Niang et al. 1998; Parola 2004).

The main arthropod vectors of SFGR are ticks, predominantly hard ticks (Ixodidae) that bite animals and humans (Luce-Fedrow et al. 2015; Parola et al. 2013). Transmission of the pathogens occurs via salivary products produced during feeding of infected vectors on the wound or mucosal surfaces. Non-validated, incompletely described, or uncultivated SFGR species have also been isolated or detected in soft ticks (Argasidae) (Parola et al. 2013); however, the competency to transmit disease is uncertain. Rickettsial infection occurs following infection of the endothelial cell lining of blood vessels (microvascular endothelium infected by R. conorii and both microvascular and macrovascular endothelium by R. rickettsii) (Colonne et al. 2011; Rydkina et al. 2010).

The purpose of this article is to discuss the distribution of SFGR in Asia, the arthropod vectors and the impact of land-use change on the spread of SFGR disease emergence.

SFGR Infection and Diagnosis

Geographical Distribution in Asia

SFGR are considered to be neglected diseases which are recently emerging or re-emerging infections in several areas of the world, especially in develo** countries across Asia (Chikeka and Dumler 2015). The distribution of SFGR based on previous reports is presented in Table 1 and Figure 1.

Table 1 Reports of spotted fever group Rickettsia spp. organisms and antibodies in humans, animals and arthropod vectors in Asia.

Figure 1

Geographical distribution of reported detections of spotted fever group Rickettsia spp. organisms and antibodies in humans, animals and arthropod vectors in Asia.

In Southeast Asia, both animals and humans are infected by SFGR. One of the earliest reports was in 1962 when Rickettsia sp. TT-118 was identified from a mixed pool of Ixodes granulatus ticks and Rhipicephalus spp. larval ticks, collected from rats (Rattus rattus) in the north region of Thailand (Chaingmai province) (Jiang et al. 2005; Robertson and Wisseman 1973). TT-118 is a homologous strain of R. honei, the pathogen of Flinders Island spotted fever (Stenos et al. 1998), and was reported in Thailand from a patient by sequencing of amplicons from five rickettsial genes to identify the species (Jiang et al. 2005). Human SFGR infection by R. honei has been reported in tropical countries such as Thailand and Malaysia (Okabayashi et al. 1996; Tay et al. 2003; Tee et al. 1999). Additionally, R. thailandii has been reported, but the pathogenic potential is not defined (Kollars et al. 2001). R. felis was first reported in Thailand in 2002 from Ctenocephalides felis, the main arthropod vector of the causative agent of cat-flea typhus or flea-borne spotted fever (Edouard et al. 2014). There are several human cases of R. felis reported in Thailand, Taiwan (Kuo et al. 2015; Lai et al. 2014; Tsai et al. 2008), Cambodia (Inpankaew et al. 2016), Japan (Perez-Osorio et al. 2008), Malaysia (Tay et al. 2014) and Laos (Dittrich et al. 2014). Besides R. felis, other SFGR have also been detected, such as R. helvetica, Rickettsia sp. AT1 and R. conorii (in particular R. conorii subsp. indica) in Laos (Dittrich et al. 2014; Phongmany et al. 2006; Varagnol et al. 2009). Rickettsia japonica, the pathogen of Japanese spotted fever infection, has been reported in Asian countries including Japan (Fournier et al. 2002), Taiwan (Tsai et al. 2008), Thailand (Okabayashi et al. 1996) and Laos (Taylor et al. 2016). In the Philippines, human antibodies against R. japonica have been reported (Camer et al. 2003). Rickettsia conorii, the causative pathogen of Mediterranean spotted fever (MSF), has been detected in Indonesia (Richards et al. 2003) and the Thailand–Burma border (Parola et al. 2003b). Three novel species were recently found in Laos which are Candidatus Rickettsia laoensis, Candidatus Rickettsia mahosotii and Candidatus Rickettsia khammouanensis (Taylor et al. 2016). In Sri Lanka, located in South Asia, SFGR R. felis, R. honei, R. conorii, R. helvetica, R. japonica and R. slovaca antibodies have been detected in both humans and canines (Kularatne et al. 2003; Nagalingam et al. 2009; Nanayakkara et al. 2013).

In Northeast/East Asia, SFGR species have been detected throughout China such as R. felis, R. sibirica, R. massiliae, R. raoultii, R. aeschlimannii, R. heiongjiangii, R. hulinii and R. mongolotimonae (Han et al. 2018; Li et al. 2018; Wei et al. 2015; Yang et al. 2016; Zhang et al. 2000, 2014). In 2015, a novel genotype of SFGR was reported as Rickettsia sp. XY99 from ill patients (Li et al. 2016). Candidatus Rickettsia gannanii and Candidatus Rickettsia barbariae were discovered and suggested to be emerging SFGR species in China (Guo et al. 2016; Yang et al. 2016). Rickettsia felis, R. japonica and other SFGR species have been identified in Hong Kong, Japan, Korea and Taiwan (Table 1) (Fournier et al. 2002; Noh et al. 2017; Slapeta et al. 2018; Tsai et al. 2008).

Seroprevalence studies have been used to determine exposure in community or hospital settings to SFGR (Table 2). In Malaysia, prevalence of TT-118 SFGR was 57.3% (Tee et al. 1999) and 12.9% (Tay and Rohani 2002). In South Korea, prevalence against R. siribica, R. conorii and R. akari was 38.6% (Jang et al. 2005). In Sri Lanka, seroprevalence studies of SFGR have found an increase in prevalence from 35 to 66% during 2000–2008 (Kularatne et al. 2013; Premaratna et al. 2008, 2014). Increasing prevalence of SFGR is also noted in central India compared to south and northeast regions (69.3%, 37.1% and 13.8%, respectively) (Kalal et al. 2016; Khan et al. 2016; Rathi et al. 2011). It should be noted that due to extensive cross-reaction within SFGR (Hechemy et al. 1989), it is generally not possible to identify the species level using serological methods unless cross-adsorption techniques are used (La Scola and Raoult 1997), and therefore, results should be interpreted with caution.

Table 2 Spotted fever group rickettsia seroprevalence studies in Asia.

SFGR Epidemiology

Vectors

In Asia, Dermacentor spp. and Haemophysalis spp. (from the family of Ixodidae, or hard ticks) are most frequently associated with rickettsial carriage in Asia, but others also include Ixodes spp., Ambylomma spp., and Rhipicephalus spp. (Table 1). Of the 22 tick species identified to carry SFGR (Table 1), their distribution is more widespread than indicated. Amblyomma testudinarium, identified in China, Japan and Laos as a vector of SFGR such as R. monacensis and R. japonica (Sun et al. 2015; Taylor et al. 2016) (Table 1), is the most widespread of the hard ticks and has also been found in India, Myanmar, Thailand, Malaysia, Indonesia, Philippines, Taiwan, Japan and Korea. Rhipicephalus sanguineus, a SFGR vector in China and India known to harbor R. conorii and R. felis (Zhang et al. 2014; Kalal et al. 2016; Sentausa et al. 2012; Parola et al. 2001), is also known for its worldwide distribution (Gray et al. 2013). The longhorned tick (Haemaphysalis longicornis) is found on livestock including cattle, pigs and chickens but also on wildlife including deer, small mammals including rats, and on cats, dogs and humans (Cane 2010). Longhorned ticks have been demonstrated to carry R. japonica (Sun et al. 2015; Lee et al. 2003), R. heilongjiangensis (Sun et al. 2015), R. rickettsii (Lee et al. 2003), Rickettsia sp. FUJ98, Rickettsia sp. HI550 and Rickettsia sp. HIR/D91 (Noh et al. 2017). It should be noted that the detection of rickettsia in the above-mentioned vectors does not imply that they are capable of transmission to hosts; therefore, it is necessary to study vector competence and capacity to better understand the threat associated with each vector.

For the Siphonaptera, Ct. felis is the most common rickettsial vector predominantly responsible for transmission of R. felis (Edouard et al. 2014; Jiang et al. 2006; Tay et al. 2014; Tsai et al. 2009; Varagnol et al. 2009; Zhang et al. 2014) and also Rickettsia sp. RF2125 (Tay et al. 2014; Kho et al. 2016). Again, Ct. felis is known to have a worldwide distribution and has been identified throughout Southeast Asia, including China, Hong Kong, Laos and Malaysia (Table 1) (Rust 2017). In addition, the fleas Ct. canis, Xenopsylla cheopsis (Jiang et al. 2006) and Vermipsylla alakurt (mainly distributed in alpine pastoral areas of Northern Asia) have all been demonstrated to be able to harbor rickettsias. Found on sheep, yaks and horses, V. alakurt has been demonstrated to be a vector for Candidatus R. barbariae (Zhao et al. 2016).

In Asia, SFGR have recently been detected in other orders although the transmission potential remains unclear. Linognathus setosus, a louse species which can be found on both domesticated and wild dogs, was found to harbor R. felis in China (Zhang et al. 2014). Mite species, although not frequently found to be infected, do remain potential biological vectors, such as Leptotrombidium delicenses which was found to harbor organisms related to R. australis and R. felis in Taiwan (Tsui et al. 2007) and is distributed throughout Southeast Asia (Lv et al. 2018). Rickettsia akari is known to be transmitted by Liponyssoides sanguineus, the house-mouse mite (Brouqui and Raoult 2006). Melophagus ovinus, the sheep ked, a native to Mongolia and North India, and introduced to Japan, was found to harbor rickettsia highly similar to R. raoultii and R. slovaca in north-western China (Liu et al. 2016).

Rickettsiae can be both transovarially and trans-staidly transmitted in vectors allowing maintenance of the pathogen within the vector population and vectors acting as reservoirs for the organisms (Parola et al. 2013). For instance with ticks, larvae, nymphs and adults are susceptible to infection and also have the capability to transmit rickettsia (Aung et al. 2014). The number of different SFGR species which a vector may harbor, and the potential for human–vector interactions is intrinsically linked to the geographic distribution of the vector and the local environment, and therefore, the distribution of SFGR is likely to be much wider than anticipated. Rhipicephalus sanguineus has been demonstrated to increase its human affinity with an increase in environmental temperature (Parola et al. 2008), and therefore, its likely significance as a clinically important vector for rickettsiosis may vary across Asia, despite being a globally distributed tick.

Hosts

Rats and other rodents are common vertebrate hosts of SFGR infections (He et al.

References

• Acestor N, Cooksey R, Newton PN, et al. (2012) Map** the aetiology of non-malarial febrile illness in Southeast Asia through a systematic review–terra incognita impairing treatment policies. PLoS One 7(9):e44269 https://doi.org/10.1371/journal.pone.0044269

• Angelakis E, Munasinghe A, Yaddehige I, et al. (2012) Detection of rickettsioses and Q fever in Sri Lanka. The American Journal of Tropical Medicine and Hygiene 86(4):711–712. https://doi.org/10.4269/ajtmh.2012.11-0424

• Aung AK, Spelman DW, Murray RJ, Graves S (2014) Rickettsial infections in Southeast Asia: implications for local populace and febrile returned travelers. Am J Trop Med Hyg 91(3):451-60 https://doi.org/10.4269/ajtmh.14-0191

• Barbara KA, Farzeli A, Ibrahim IN, et al. (2010) Rickettsial infections of fleas collected from small mammals on four islands in Indonesia. J Med Entomol 47(6):1173-8

• Bhengsri S, Baggett HC, Edouard S, et al. (2016) Sennetsu Neorickettsiosis, Spotted Fever Group, and Typhus Group Rickettsioses in Three Provinces in Thailand. Am J Trop Med Hyg 95(1):43-9 https://doi.org/10.4269/ajtmh.15-0752

• Brouqui P, Raoult D (2006) Arthropod-borne diseases in homeless. Ann N Y Acad Sci 1078:223-35 https://doi.org/10.1196/annals.1374.041

• Burnside WR, Brown JH, Burger O, Hamilton MJ, Moses M, Bettencourt LM (2012) Human macroecology: linking pattern and process in big-picture human ecology. Biol Rev Camb Philos Soc 87(1):194-208 https://doi.org/10.1111/j.1469-185x.2011.00192.x

• Camer GA, Alejandria M, Amor M, et al. (2003) Detection of antibodies against spotted fever group Rickettsia (SFGR), typhus group Rickettsia (TGR), and Coxiella burnetii in human febrile patients in the Philippines. Jpn J Infect Dis 56(1):26-8

• Cane R (2010) Haemaphysalis longicornis Neumann, 1901 In: Profile New Zealand Biosecure Entomology Laboratory. https://www.smsl.co.nz/site/southernmonitoring/files/NZB/Ha%20longicornis%20Profile.pdf. Accessed 4 December 2018

• Chikeka I, Dumler JS (2015) Neglected bacterial zoonoses. Clin Microbiol Infect 21(5):404-15 https://doi.org/10.1016/j.cmi.2015.04.022

• Choi YJ, Jang WJ, Ryu JS, et al. (2005) Spotted fever group and typhus group rickettsioses in humans, South Korea. Emerging Infectious Diseases 11(2):237–244. https://doi.org/10.3201/eid1102.040603

• Clements GR, Lynam AJ, Gaveau D, et al. (2014) Where and how are roads endangering mammals in Southeast Asia’s forests? PLoS One 9(12):e115376 https://doi.org/10.1371/journal.pone.0115376

• Colonne PM, Eremeeva ME, Sahni SK (2011) Beta interferon-mediated activation of signal transducer and activator of transcription protein 1 interferes with Rickettsia conorii replication in human endothelial cells. Infect Immun 79(9):3733-43 https://doi.org/10.1128/iai.05008-11

• Cropper M, Puri J, Griffiths C (2001) Predicting the location of deforestation: the role of roads and protected areas in North Thailand. Land Econ 77:172–186.

• Dittrich S, Phommasone K, Anantatat T, et al. (2014) Rickettsia felis Infections and comorbid conditions, Laos, 2003-2011. Emerg Infect Dis 20(8):1402-4 https://doi.org/10.3201/eid2008.131308

• Edouard S, Bhengsri S, Dowell SF, Watt G, Parola P, Raoult D (2014) Two human cases of Rickettsia felis infection, Thailand. Emerg Infect Dis 20(10):1780-1 https://doi.org/10.3201/eid2010.140905

• FAO (2005) Global Forest Resources Assessment 2005 FAO Forestry Paper 147

• Faruque LI, Zaman RU, Gurley ES, et al. (2017) Prevalence and clinical presentation of Rickettsia, Coxiella, Leptospira, Bartonella and chikungunya virus infections among hospital-based febrile patients from December 2008 to November 2009 in Bangladesh. BMC Infect Dis 17(1):141 https://doi.org/10.1186/s12879-017-2239-6

• Finch C, Al-Damluji MS, Krause PJ, Niccolai L, Steeves T, O'Keefe CF, Diuk-Wasser MA (2014) Integrated assessment of behavioral and environmental risk factors for Lyme disease infection on Block Island, Rhode Island. PLoS ONE 9:e84758

• Foley JA, Defries R, Asner GP, et al. (2005) Global consequences of land use. Science 309(5734):570-4 https://doi.org/10.1126/science.1111772

• Fournier PE, Fujita H, Takada N, Raoult D (2002) Genetic identification of rickettsiae isolated from ticks in Japan. J Clin Microbiol 40(6):2176-81

• Fournier PE, Raoult D (2009) Current knowledge on phylogeny and taxonomy of Rickettsia spp. Ann N Y Acad Sci 1166:1-11 https://doi.org/10.1111/j.1749-6632.2009.04528.x

• Gillespie JJ, Williams K, Shukla M, et al. (2008) Rickettsia phylogenomics: unwinding the intricacies of obligate intracellular life. PLoS One 3(4):e2018 https://doi.org/10.1371/journal.pone.0002018

• Graves S, Stenos J (2009) Rickettsioses in Australia. Ann N Y Acad Sci 1166:151-5 https://doi.org/10.1111/j.1749-6632.2009.04530.x

• Gray J, Dantas-Torres F, Estrada-Pena A, Levin M (2013) Systematics and ecology of the brown dog tick, Rhipicephalus sanguineus. Ticks Tick Borne Dis 4(3):171-80 https://doi.org/10.1016/j.ttbdis.2012.12.003

• Guo LP, Jiang SH, Liu D, Wang SW, Chen CF, Wang YZ (2016) Emerging spotted fever group rickettsiae in ticks, northwestern China. Ticks Tick Borne Dis 7(6):1146-1150 https://doi.org/10.1016/j.ttbdis.2016.08.006

• Haddad NM, Brudvig LA, Clobert J, et al. (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1(2):e1500052 https://doi.org/10.1126/sciadv.1500052

• Han R, Yang J, Niu Q, et al. (2018) Molecular prevalence of spotted fever group rickettsiae in ticks from Qinghai Province, northwestern China. Infect Genet Evol 57:1-7 https://doi.org/10.1016/j.meegid.2017.10.025

• He JF, Zheng K, Li W, et al. (2003) [Study on spotted fever group Rickettsiae in Guangdong province]. Zhonghua Liu **ng Bing Xue Za Zhi 24(8):700-3

• Hechemy KE, Raoult D, Fox J, Han Y, Elliott LB, Rawlings J (1989) Cross-reaction of immune sera from patients with rickettsial diseases. J Med Microbiol 29(3):199-202 https://doi.org/10.1099/00222615-29-3-199

• Imaoka K, Kaneko S, Tabara K, Kusatake K, Morita E (2011) The First Human Case of Rickettsia tamurae Infection in Japan. Case Reports in Dermatology 3(1):68–73. https://doi.org/10.1159/000326941

• Inpankaew T, Hii SF, Chimnoi W, Traub RJ (2016) Canine vector-borne pathogens in semi-domesticated dogs residing in northern Cambodia. Parasit Vectors 9(1):253 https://doi.org/10.1186/s13071-016-1552-z

• Ishiguro F, Takada N, Fujita H, Noji Y, Yano Y, Iwasaki H (2008) Survey of the vectorial competence of ticks in an endemic area of spotted fever group rickettsioses in Fukui Prefecture, Japan. Microbiology and Immunology 52(6):305–309. https://doi.org/10.1111/j.1348-0421.2008.00042.x

• Izzard L, Fuller A, Blacksell SD, et al. (2010) Isolation of a novel Orientia species (O. chuto sp. nov.) from a patient infected in Dubai. J Clin Microbiol 48(12):4404-9 https://doi.org/10.1128/jcm.01526-10

• Jang WJ, Choi YJ, Kim JH, et al. (2005) Seroepidemiology of spotted fever group and typhus group rickettsioses in humans, South Korea. Microbiol Immunol 49(1):17-24

• Jiang J, Sangkasuwan V, Lerdthusnee K, et al. (2005) Human Infection with Rickettsia honei, Thailand. Emerg Infect Dis 11(9):1473-5 https://doi.org/10.3201/eid1109.050111

• Jiang J, Soeatmadji DW, Henry KM, Ratiwayanto S, Bangs MJ, Richards AL (2006) Rickettsia felis in Xenopsylla cheopis, Java, Indonesia. Emerg Infect Dis 12(8):1281-3 https://doi.org/10.3201/eid1208.060327

• Jones KE, Patel NG, Levy MA, et al. (2008) Global trends in emerging infectious diseases. Nature 451(7181):990-3 https://doi.org/10.1038/nature06536

• Kalal BS, Puranik P, Nagaraj S, Rego S, Shet A (2016) Scrub typhus and spotted fever among hospitalised children in South India: Clinical profile and serological epidemiology. Indian J Med Microbiol 34(3):293-8 https://doi.org/10.4103/0255-0857.188315

• Kato CY, Chung IH, Robinson LK, Austin AL, Dasch GA, Massung RF (2013) Assessment of real-time PCR assay for detection of Rickettsia spp. and Rickettsia rickettsii in banked clinical samples. Journal of Clinical Microbiology 51(1):314-7 https://doi.org/10.1128/jcm.01723-12

• Keesing F, Belden LK, Daszak P, et al. (2010) Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468(7324):647-52 https://doi.org/10.1038/nature09575

• Khan SA, Bora T, Chattopadhyay S, Jiang J, Richards AL, Dutta P (2016) Seroepidemiology of rickettsial infections in Northeast India. Trans R Soc Trop Med Hyg 110(8):487-94 https://doi.org/10.1093/trstmh/trw052

• Kho KL, Koh FX, Hasan LI, et al. (2017) Rickettsial seropositivity in the indigenous community and animal farm workers, and vector surveillance in Peninsular Malaysia. Emerging Microbes & Infections 6(4):e18. https://doi.org/10.1038/emi.2017.4

• Kho KL, Koh FX, Singh HKL, Zan HAM, Ponnampalavanar S, Kukreja A, Tay ST (2016) Spotted fever group rickettsioses and murine typhus in a Malaysian teaching hospital. The American Journal of Tropical Medicine and Hygiene 95:765–768. https://doi.org/10.4269/ajtmh.16-0199

• Kollars TM, Jr., Tippayachai B, Bodhidatta D (2001) Short report: Thai tick typhus, Rickettsia honei, and a unique rickettsia detected in Ixodes granulatus (Ixodidae: Acari) from Thailand. Am J Trop Med Hyg 65(5):535-7

• Kularatne SA, Edirisingha JS, Gawarammana IB, Urakami H, Chenchittikul M, Kaiho I (2003) Emerging rickettsial infections in Sri Lanka: the pattern in the hilly Central Province. Trop Med Int Health 8(9):803-11

• Kularatne SA, Rajapakse RP, Wickramasinghe WM, et al. (2013) Rickettsioses in the central hills of Sri Lanka: serological evidence of increasing burden of spotted fever group. Int J Infect Dis 17(11):e988-92 https://doi.org/10.1016/j.ijid.2013.05.014

• Kuo CC, Huang JL, Lin TE, Wang HC (2012) Detection of Rickettsia spp. and host and habitat associations of fleas (Siphonaptera) in eastern Taiwan. Med Vet Entomol 26(3):341–350. https://doi.org/10.1111/j.1365-2915.2012.01009.x

• Kuo CC, Lin YF, Yao CT, et al. (2017) Tick-borne pathogens in ticks collected from birds in Taiwan. Parasit Vectors 10(1):587 https://doi.org/10.1186/s13071-017-2535-4

• Kuo CC, Shu PY, Mu JJ, Wang HC (2015) High prevalence of Rickettsia infections in small mammals in Taiwan. Vector Borne Zoonotic Dis 15(1):13-20. https://doi.org/10.1089/vbz.2014.1584

• La Scola B, Raoult D (1997) Laboratory diagnosis of rickettsioses: current approaches to diagnosis of old and new rickettsial diseases. J Clin Microbiol 35(11):2715-27

• Lai CH, Chang LL, Lin JN, et al. (2014) Human spotted fever group rickettsioses are underappreciated in southern Taiwan, particularly for the species closely-related to Rickettsia felis. PLoS One 9(4):e95810 https://doi.org/10.1371/journal.pone.0095810

• Laurance WF, Albernaz AKM, Schroth G, et al. (2002) Predictors of deforestation in the Brazilian Amazon. J Biogeogr 29:737–748

• Lee JH, Park HS, Jung KD, et al. (2003) Identification of the spotted fever group rickettsiae detected from Haemaphysalis longicornis in Korea. Microbiology and Immunology 47(4):301–304

• Levin ML (2018) Ambylomma spp. In: MSD Manual: Veterinary Manual. https://www.msdvetmanual.com/integumentary-system/ticks/amblyomma-spp. Accessed 10 December 2018

• Li H, Cui XM, Cui N, et al. (2016) Human Infection with Novel Spotted Fever Group Rickettsia Genotype, China, 2015. Emerg Infect Dis 22(12):2153-2156 https://doi.org/10.3201/eid2212.160962

• Li H, Zhang PH, Huang Y, et al. (2018) Isolation and Identification of Rickettsia raoultii in Human Cases: A Surveillance Study in 3 Medical Centers in China. Clin Infect Dis 66(7):1109-1115 https://doi.org/10.1093/cid/cix917

• Liu D, Wang YZ, Zhang H, et al. (2016) First report of Rickettsia raoultii and in Melophagus ovinus, the sheep ked. Parasites and Vectors 9(1):600. https://doi.org/10.1186/s13071-016-1885-7

• Luce-Fedrow A, Mullins K, Kostik AP, St John HK, Jiang J, Richards AL (2015) Strategies for detecting rickettsiae and diagnosing rickettsial diseases. Future Microbiol 10(4):537-64 https://doi.org/10.2217/fmb.14.141

• Lv Y, Guo XG, ** DC (2018) Research Progress on Leptotrombidium deliense. Korean J Parasitol 56(4):313-324 https://doi.org/10.3347/kjp.2018.56.4.313

• Lynn MS, William T, Tanganuchitcharnchai A, et al. (2018) Spotted fever rickettsiosis in a wildlife researcher in Sabah, Malaysia: a case study. Tropical Medicine and Infectious Disease 3(1):1

• Ma SK, Wong WC, Leung CW, et al. (2011) Review of vector-borne diseases in Hong Kong. Travel Med Infect Dis 9(3):95-105 https://doi.org/10.1016/j.tmaid.2010.01.004

• Mahara F (1997) Japanese spotted fever: report of 31 cases and review of the literature. Emerging Infectious Diseases 3(2):105–111. https://doi.org/10.3201/eid0302.970203

• Merhej V, Angelakis E, Socolovschi C, Raoult D (2014) Genoty**, evolution and epidemiological findings of Rickettsia species. Infect Genet Evol 25:122-37 https://doi.org/10.1016/j.meegid.2014.03.014

• Miyamoto M (2006) Forest conversion to rubber around Sumatran villages in Indonesia: comparing the impacts of road construction, transmigration projects and population. Forest Policy Econ 9:1-12

• Myers SS, Patz JA (2009) Emerging Threats to Human Health from Global Environmental Change. Annual Review of Environment and Resources 34(1):223-252

• Nagalingam K, Rolain JM, Thevanesam V, Lakkumar F, Gunawardana G, Raoult D (2009) Spotted fever rickettsioses in children in Sri Lanka. Clin Microbiol Infect 15 Suppl 2:330-1 https://doi.org/10.1111/j.1469-0691.2008.02262.x

• Nanayakkara DM, Rajapakse RP, Wickramasinghe S, Kularatne SA (2013) Serological evidence for exposure of dogs to Rickettsia conorii, Rickettsia typhi, and Orientia tsutsugamushi in Sri Lanka. Vector Borne Zoonotic Dis 13(8):545-9 https://doi.org/10.1089/vbz.2012.1049

• Niang M, Parola P, Tissot-Dupont H, Baidi L, Brouqui P, Raoult D (1998) Prevalence of antibodies to Rickettsia conorii Ricketsia africae, Rickettsia typhi and Coxiella burnetii in Mauritania. Eur J Epidemiol 14(8):817-8

• Noh Y, Lee YS, Kim HC, et al. (2017) Molecular detection of Rickettsia species in ticks collected from the southwestern provinces of the Republic of Korea. Parasit Vectors 10(1):20 https://doi.org/10.1186/s13071-016-1955-x

• Okabayashi T, Tsutiya K, Muramatsu Y, Ueno H, Morita C (1996) Serological survey of spotted fever group rickettsia in wild rats in Thailand in the 1970s. Microbiol Immunol 40(12):895-8

• Parola P (2004) Tick-borne rickettsial diseases: emerging risks in Europe. Comp Immunol Microbiol Infect Dis 27(5):297-304 https://doi.org/10.1016/j.cimid.2004.03.006

• Parola P, Cornet JP, Sanogo YO, et al. (2003a) Detection of Ehrlichia spp., Anaplasma spp., Rickettsia spp., and other eubacteria in ticks from the Thai-Myanmar border and Vietnam. Journal of Clinical Microbiology 41(4):1600-8

• Parola P, Fenollar F, Badiaga S, Brouqui P, Raoult D (2001) First documentation of Rickettsia conorii infection (strain Indian tick typhus) in a Traveler. Emerg Infect Dis 7(5):909-10 https://doi.org/10.3201/eid0705.017527

• Parola P, Miller RS, McDaniel P, et al. (2003b) Emerging rickettsioses of the Thai-Myanmar border. Emerg Infect Dis 9(5):592-5

• Parola P, Paddock CD, Socolovschi C, et al. (2013) Update on tick-borne rickettsioses around the world: a geographic approach. Clin Microbiol Rev 26(4):657-702 https://doi.org/10.1128/cmr.00032-13

• Parola P, Socolovschi C, Jeanjean L, et al. (2008) Warmer weather linked to tick attack and emergence of severe rickettsioses. PLoS Negl Trop Dis 2(11):e338 https://doi.org/10.1371/journal.pntd.0000338

• Patz JA, Daszak P, Tabor GM, et al. (2004) Unhealthy landscapes: Policy recommendations on land use change and infectious disease emergence. Environ Health Perspect 112(10):1092-8

• Perez-Osorio CE, Zavala-Velazquez JE, Arias Leon JJ, Zavala-Castro JE (2008) Rickettsia felis as emergent global threat for humans. Emerg Infect Dis 14(7):1019-23 https://doi.org/10.3201/eid1407.071656

• Phongmany S, Rolain JM, Phetsouvanh R, et al. (2006) Rickettsial infections and fever, Vientiane, Laos. Emerg Infect Dis 12(2):256-62 https://doi.org/10.3201/eid1202.050900

• PicKard AL, McDaniel P, Miller RS, et al. (2004) A study of’febrile illnesses on the Thai-Myanmar border: predictive factors of rickettsioses. Southeast Asian J Trop Med Public Health 35(3):657-63

• Premaratna R (2016) Epidemiology and ecology of rickettsial Infections. International Journal of Infectious Diseases 45S 1–477

• Premaratna R, Ariyaratna N, Attanayake C, Bandara W, Chandrasena N, de Silva HJ (2014) Rickettsial infection among military personnel deployed in Northern Sri Lanka. BMC Infect Dis 14:3864 https://doi.org/10.1186/s12879-014-0688-8

• Premaratna R, Loftis AD, Chandrasena TG, Dasch GA, de Silva HJ (2008) Rickettsial infections and their clinical presentations in the Western Province of Sri Lanka: a hospital-based study. Int J Infect Dis 12(2):198-202 https://doi.org/10.1016/j.ijid.2007.06.009

• Quintero VJ, Paternina TL, Uribe YA, et al. (2017) Eco-epidemiological analysis of rickettsial seropositivity in rural areas of Colombia: A multilevel approach. PLoS Negl Trop Dis 11(9):e0005892 https://doi.org/10.1371/journal.pntd.0005892

• Ramankutty N, Foley J (1999) Estimating historical changes in global land cover: Croplands from 1700 to 1992. Global Biogeochemical Cycles 13(4):997-1027

• Rathi NB, Rathi AN, Goodman MH, Aghai ZH (2011) Rickettsial diseases in central India: proposed clinical scoring system for early detection of spotted fever. Indian Pediatr 48(11):867-72

• Richards AL, Ratiwayanto S, Rahardjo E, et al. (2003) Serologic evidence of infection with ehrlichiae and spotted fever group rickettsiae among residents of Gag Island, Indonesia. Am J Trop Med Hyg 68(4):480-4

• Robertson RG, Wisseman CL, Jr. (1973) Tick-borne rickettsiae of the spotted fever group in West Pakistan. II. Serological classification of isolates from West Pakistan and Thailand: evidence for two new species. Am J Epidemiol 97(1):55-64

• Rodkvamtook W, Gaywee J, Kanjanavanit S, et al. (2013) Scrub typhus outbreak, northern Thailand, 2006-2007. Emerg Infect Dis 19(5):774-7 https://doi.org/10.3201/eid1905.121445

• Rust MK (2017) The Biology and Ecology of Cat Fleas and Advancements in Their Pest Management: A Review. Insects 8(4) https://doi.org/10.3390/insects8040118

• Rydkina E, Turpin LC, Sahni SK (2010) Rickettsia rickettsii infection of human macrovascular and microvascular endothelial cells reveals activation of both common and cell type-specific host response mechanisms. Infect Immun 78(6):2599-606 https://doi.org/10.1128/iai.01335-09

• Satoh H, Tsuneki A, Inokuma H, Kumazawa N, Jahana Y, Kiyuuna T, Okabayashi T, Muramatsu Y, Ueno H, Morita C (2001) Seroprevalence of antibodies against spotted fever group rickettsia among dogs and humans in Okinawa, Japan. Microbiology and Immunology 45:85–87

• Scientific Committee on Vector-borne Diseases (2013) Epidemiology, Prevention and Control of Spotted Fever in Hong Kong

• Scinachi CA, Takeda G, Mucci LF, Pinter A (2017) Association of the occurrence of Brazilian spotted fever and Atlantic rain forest fragmentation in the Sao Paulo metropolitan region, Brazil. Acta Trop 166:225-233 https://doi.org/10.1016/j.actatropica.2016.11.025

• Sentausa E, El Karkouri K, Robert C, Raoult D, Fournier PE (2012) Genome sequence of Rickettsia conorii subsp. indica, the agent of Indian tick typhus. J Bacteriol 194(12):3288-9 https://doi.org/10.1128/jb.00462-12

• Slapeta J, Lawrence A, Reichel MP (2018) Cat fleas (Ctenocephalides felis) carrying Rickettsia felis and Bartonella species in Hong Kong. Parasitol Int 67(2):209-212 https://doi.org/10.1016/j.parint.2017.12.001

• Stenos J, Roux V, Walker D, Raoult D (1998) Rickettsia honei sp. nov., the aetiological agent of Flinders Island spotted fever in Australia. Int J Syst Bacteriol 48 Pt 4:1399-404 https://doi.org/10.1099/00207713-48-4-1399

• Sun J, Lin J, Gong Z, et al. (2015) Detection of spotted fever group Rickettsiae in ticks from Zhejiang Province, China. Exp Appl Acarol 65(3):403-11 https://doi.org/10.1007/s10493-015-9880-9

• Tay ST, Ho TM, Rohani MY, Devi S (2000) Antibodies to Orientia tsutsugamushi, Rickettsia typhi and spotted fever group rickettsiae among febrile patients in rural areas of Malaysia. Trans R Soc Trop Med Hyg 94(3):280-4

• Tay ST, Kamalanathan M, Rohani MY (2003) Antibody prevalence of Orientia tsutsugamushi, Rickettsia typhi and TT118 spotted fever group rickettsiae among Malaysian blood donors and febrile patients in the urban areas. Southeast Asian J Trop Med Public Health 34(1):165-70

• Tay ST, Koh FX, Kho KL, Sitam FT (2015) Rickettsial infections in monkeys, Malaysia. Emerg Infect Dis 21(3):545-7 https://doi.org/10.3201/eid2103.141457

• Tay ST, Mokhtar AS, Low KC, et al. (2014) Identification of rickettsiae from wild rats and cat fleas in Malaysia. Med Vet Entomol 28 Suppl 1:104-8 https://doi.org/10.1111/mve.12075

• Tay ST, Rohani MY (2002) The use of the indirect immunoperoxidase test for the serodiagnosis of rickettsial diseases in Malaysia. Southeast Asian J Trop Med Public Health 33(2):314-20

• Taylor AJ, Vongphayloth K, Vongsouvath M, et al. (2016) Large-Scale Survey for Tickborne Bacteria, Khammouan Province, Laos. Emerg Infect Dis 22(9):1635-9 https://doi.org/10.3201/eid2209.151969

• Taylor LH, Latham SM, Woolhouse ME (2001) Risk factors for human disease emergence. Philos Trans R Soc Lond B Biol Sci 356(1411):983-9 https://doi.org/10.1098/rstb.2001.0888

• Tee TS, Kamalanathan M, Suan KA, et al. (1999) Seroepidemiologic survey of Orientia tsutsugamushi, Rickettsia typhi, and TT118 spotted fever group rickettsiae in rubber estate workers in Malaysia. Am J Trop Med Hyg 61(1):73-7

• Trung NV, Hoi LT, Thuong NTH, et al. (2017) Seroprevalence of Scrub Typhus, Typhus, and Spotted Fever Among Rural and Urban Populations of Northern Vietnam. Am J Trop Med Hyg 96(5):1084-1087 https://doi.org/10.4269/ajtmh.16-0399

• Tsai KH, Lu HY, Huang JH, et al. (2009) African tick bite Fever in a Taiwanese traveler returning from South Africa: molecular and serologic studies. Am J Trop Med Hyg 81(5):735-9 https://doi.org/10.4269/ajtmh.2009.09-0101

• Tsai KH, Lu HY, Tsai JJ, Yu SK, Huang JH, Shu PY (2008) Human case of Rickettsia felis infection, Taiwan. Emerg Infect Dis 14(12):1970-2 https://doi.org/10.3201/eid1412.080515

• Tsui PY, Tsai KH, Weng MH, et al. (2007) Molecular detection and characterization of spotted fever group rickettsiae in Taiwan. Am J Trop Med Hyg 77(5):883-90

• Vallee J, Thaojaikong T, Moore CE, et al. (2010) Contrasting spatial distribution and risk factors for past infection with scrub typhus and murine typhus in Vientiane City, Lao PDR. PLoS Negl Trop Dis 4(12):e909 https://doi.org/10.1371/journal.pntd.0000909

• Varagnol M, Parola P, Jouan R, Beaucournu JC, Rolain JM, Raoult D (2009) First detection of Rickettsia felis and Bartonella clarridgeiae in fleas from Laos. Clin Microbiol Infect 15 Suppl 2:334-5 https://doi.org/10.1111/j.1469-0691.2008.02272.x

• Vitorino L, Chelo IM, Bacellar F, Ze-Ze L (2007) Rickettsiae phylogeny: a multigenic approach. Microbiology 153(Pt 1):160-8 https://doi.org/10.1099/mic.0.2006/001149-0

• Watson JEM, Evans T, Venter O, et al. (2018) The exceptional value of intact forest ecosystems. Nat Ecol Evol 2(4):599-610 https://doi.org/10.1038/s41559-018-0490-x

• Wei QQ, Guo LP, Wang AD, et al. (2015) The first detection of Rickettsia aeschlimannii and Rickettsia massiliae in Rhipicephalus turanicus ticks, in northwest China. Parasit Vectors 8:631 https://doi.org/10.1186/s13071-015-1242-2

• Worldometers (2018) Asia Population. In. http://www.worldometers.info/world-population/asia-population. Accessed 30 May 2018

• Yang J, Tian Z, Liu Z, et al. (2016) Novel spotted fever group rickettsiae in Haemaphysalis qinghaiensis ticks from Gansu, Northwest China. Parasit Vectors 9:146 https://doi.org/10.1186/s13071-016-1423-7

• Zhang J, Lu G, Kelly P, et al. (2014) First report of Rickettsia felis in China. BMC Infect Dis 14:682 https://doi.org/10.1186/s12879-014-0682-1

• Zhang JZ, Fan MY, Wu YM, Fournier PE, Roux V, Raoult D (2000) Genetic classification of “Rickettsia heilongjiangii” and “Rickettsia hulinii,” two Chinese spotted fever group rickettsiae. J Clin Microbiol 38(9):3498-501

• Zhao SS, Li HY, Yin XP, Liu ZQ, Chen CF, Wang YZ (2016) First detection of Candidatus Rickettsia barbariae in the flea Vermipsylla alakurt from north-western China. Parasit Vectors 9(1):325 https://doi.org/10.1186/s13071-016-1614-2

Acknowledgements

Stuart Blacksell and Matthew Robinson are funded by the Wellcome Trust of the United Kingdom. We wish to thank Paul Bloxham for the maps used in this publication.

Author information

Authors and Affiliations

1. Mahidol-Oxford Tropical Medicine Research Unit, Faculty of Tropical Medicine, Mahidol University, 420/6 Rajvithee Road, Bangkok, 10400, Thailand

   Jaruwan Satjanadumrong, Tom Hughes & Stuart D. Blacksell

2. Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit (LOMWRU), Mahosot Hospital, Vientiane, Lao People’s Democratic Republic

   Matthew T. Robinson & Stuart D. Blacksell

3. Centre for Tropical Medicine and Global Health, Nuffield Department of Clinical Medicine, Churchill Hospital, University of Oxford, Oxford, OX3 7FZ, UK

   Matthew T. Robinson & Stuart D. Blacksell

4. EcoHealth Alliance, 460 West 34th Street, 17th Floor, New York, NY, USA

   Tom Hughes

Corresponding author

Correspondence to Stuart D. Blacksell.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Reprints and permissions

About this article

Cite this article

Satjanadumrong, J., Robinson, M.T., Hughes, T. et al. Distribution and Ecological Drivers of Spotted Fever Group Rickettsia in Asia. EcoHealth 16, 611–626 (2019). https://doi.org/10.1007/s10393-019-01409-3

• Received: 04 June 2018

• Revised: 21 February 2019

• Accepted: 22 February 2019

• Published: 15 April 2019

• Issue Date: December 2019

• DOI: https://doi.org/10.1007/s10393-019-01409-3

Keywords