TICK-BORNE PATHOGENS IN THAILAND
REVIEW
TICK-BORNE PATHOGENS AND DISEASES OF ANIMALS AND HUMANS IN THAILAND
A Ahantarig, W Trinachartvanit and JR Milne
Department of Biology, Faculty of Science, Mahidol University, Bangkok, Thailand
Abstract. Tick-borne pathogens in Thailand can cause diseases that result in productivity and economic losses in the livestock sector as well as cause debilitating illnesses in humans and their companion animals. With the advent of molecular techniques, accurate identification of tick-borne pathogens and precise diagnosis of disease is now available. This literature review summarizes the various tick-borne pathogens that have been isolated from ticks and their vertebrate hosts in Thailand, covering those protozoa, rickettsiae, bacteria and viruses most responsible for human and veterinary disease with particular emphasis on those that have been characterized molecularly.
INTRODUCTION 1997). High standards of quality control for farm animals and meat products, including Ticks are surpassed only by mosquitoes disease preventions, are essential to sustain as arthropod vectors of disease (Dennis and this expanding industry. The increasing popu- Piesman, 2005). A wide variety of pathogens larity of pet ownership together with the ex- that can be propagated and transmitted by istence of large populations of stray dogs and ticks commonly infect both humans and ani- cats in Southeast Asian countries including mals found in close association with man (eg, Thailand provide an ideal environment for tick- cattle, dogs, cats, rodents and fowl). Tick- borne disease transmission to humans and borne pathogens in Thailand involve protozoa, companion animals (Irwin and Jefferies, 2004). rickettsiae, bacteria and Flavivirus species and The accurate detection of tick-borne cause diseases such as anaplasmosis, babe- pathogens is an important aspect of livestock siosis, ehrlichiosis and rickettsiosis. Small- quality control as well as disease diagnosis. scale livestock industry is expanding in this Assays based on microscopic or serological country because of a demand from national examination are often not sensitive enough to markets and an export-based economy. Tick- detect pathogens, especially when they oc- borne diseases will assume an increasingly cur at low infection levels. In addition, the lack greater importance and necessity for control of microscopic distinguishing features among as the demand for meat and other animal pathogen species or the always-present prob- products continues to increase with the im- lem of cross-reactivity in serological tests provement of Thailand’s economy (Chansiri, makes accurate identification at the species level difficult. With the advent of molecular di- Correspondence: Dr Arunee Ahantarig, Department of Biology, Faculty of Science, Mahidol University, agnostic techniques in the 1990’s, sensitive Rama VI Road, Bangkok 10400, Thailand. and accurate determinations of pathogen spe- Tel: +66 (0) 2201 5380, Fax: +66 (0) 2354 7161 cies can now be performed. E-mail: [email protected] This review summarizes the various
Vol 39 No. 6 November 2008 1015 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH tick-borne pathogens that have been isolated reactions between B. bigemina and B. bovis from ticks and their vertebrate hosts in Thai- (Wright et al, 1987; Figueroa et al, 1992). Mo- land. In particular, we concentrate on those lecular techniques have often been developed pathogens that have been detected and char- to overcome the problem of serological cross- acterized using molecular techniques (Tables reactivity among closely related pathogens. In 1 and 2). This review presents an update of Thailand, a molecular technique for specifically those pathogens borne by ticks that have detecting B. bovis in cattle was developed in been detected both in ticks and various ver- 1992 (Petchpoo et al, 1992) and other tech- tebrate species, including humans, in Thai- niques have been reported more recently land. Future needs for determining the extent (Thammasirirak et al, 2003; Patarapadungkit of the tick-borne pathogen problem in this et al, 2004). Nevertheless, the extent to which country are discussed. these methods have been used, eg, in deter- mining the prevalences of the two bovine Ba- PROTOZOAL PATHOGENS besia species, is unknown because of the lack of published reports that use them. Babesia The prevalence of Babesia infections in Babesiosis is an emerging tick-transmit- Thai cattle is highly variable (Nishikawa et al, ted, zoonotic disease of worldwide economic, 1990; Phrikanahok et al, 2000) but in some medical and veterinary importance. It is areas seropositives as high as 96.7% have caused by intra-erythrocytic parasites of the been reported (Nishikawa et al, 1990). Im- genus Babesia (Homer et al, 2000). Babesia ported cattle and their hybrid offspring appear spp infect many types of mammals, especially to be more susceptible to Babesia infection in the order Rodentia, as well as some spe- than native breeds (Tan-Ariya et al, 1992). cies of birds. The manifestations of the dis- However, even native breeds may be suscep- ease are broad, ranging from silent infesta- tible if raised in a babesiosis-free area and then tion to a fulminant malaria-like disease result- exposed to cattle from a babesiosis-endemic ing in severe hemolysis and death. In Thai- area (Pemayodhin et al, 1991). Rhipicephalus land, Babesia parasites have been found in (formerly Boophilus) microplus is the recog- cattle, dogs and a species of rodent nized tick vector of both B. bovis and B. (Bandicota indica) (Table 1) as well as in cats bigemina throughout the world (Bock et al, (Jittapalapong and Jansawan, 1993) and a 2004). This tick species is widespread in Thai- species of bird (Dendrocitta vagabunda; land (Tanskul et al, 1983) and a recent study Peirce, 2000). confirmed infection by the parasite, B. Bovine babesiosis in particular threatens bigemina, in 45.6% of tick individuals collected the cattle industry in tropical and sub-tropical from cattle in an enzootic area of Thailand regions, and production of cattle and buffa- (Jittapalapong et al, 2004). loes in many Asian countries, including Thai- In Thai dogs, one species of Babesia, land, has been impaired by this lethal disease namely B. canis, has been associated with (Brockelman, 1989, cited in Tan-Ariya et al, canine babesiosis (Table 1). Although antigens 1992). The important causative agents of bo- to another species, B. gibsonii, have been vine babesiosis in Asia are B. bovis and B. detected, infection by the latter cannot be con- bigemina (Bock et al, 2004). However, the se- firmed by molecular methods (Suksawat et al, rological techniques used to diagnose bovine 2001a). B. canis is separated into three sub- babesiosis do not consistently detect carrier species based on differences in vector speci- animals and do not specifically eliminate cross- ficity, cross-immunity and pathogenicity
1016 Vol 39 No. 6 November 2008 TICK-BORNE PATHOGENS IN THAILAND among isolates (Uilenberg, 2006) and these no ambiguities resulting from direct sequenc- along with molecular differences have resulted ing of the PCR products (Dantrakool et al, in proposals to call them separate species 2004). More than half (17/33) of the rodents (Zahler et al, 1998). However, there has not were found to have Babesia in their blood. yet been any consensus among taxonomists Haemaphysalis doenitzi ticks were identified regarding the taxonomy of the B. canis group. exclusively on Babesia-positive Bandicota in- The B. canis that occurs in Southeast Asia, dica, so this tick species may prove to be the sometimes referred to as subspecies vogelli vector. (Irwin and Jefferies, 2004), is transmitted by the In other parts of the world, babesiosis in brown dog tick Rhipicephalus sanguineus humans has been diagnosed initially as ma- (Shaw et al, 2001a), a tick that is commonly laria (Dantrakool et al, 2004). Thus, it is prob- found on Thai dogs (Tanskul et al, 1983). able that cases of human babesiosis in coun- Among pet dogs of Samut Prakan Province tries like Thailand, in which malaria is endemic, near Bangkok, 3.75% were infected with Ba- have been overlooked or misdiagnosed as besia based on hematological characteristics malaria. Human Babesia is considered to (Jittapalapong and Tipsawake, 1991). A simi- come from rodents alongside humans lar rate (3.07%) was determined for canine (Dantrakool et al, 2004). The fact that Babe- blood samples submitted to a Kamphaeng sia has been found in a Thai rodent, that Ba- Saen animal hospital northwest of Bangkok besia tick vectors like Rhipicephalus microplus (Salakij et al, 1999). A much higher Babesia and Rhipicephalus sanguineus occur in Thai- infection rate is expected in populations of stray land and sometimes infest people (Estrada- dogs throughout Thailand because of their Pena and Jongejan 1999) and that first de- greater exposure to ticks. tections of human babesiosis have recently Babesia infection has also been detected been reported from other Asian countries, in- in equine animals in Thailand with 1 and 62 cluding Taiwan, Japan and Korea (Shih et al, out of 400 tested horses, donkeys and mules 1997; Saito-Ito et al, 2000; Kim et al, 2007) being seropositive for B. caballi and B. equi, emphasizes the importance of continual sur- respectively (Tantaswasdi et al, 1998). Despite veillance for human babesiosis in Thailand. the high prevalence of parasites, there have Theileria been no clinical reports of the disease equine Protozoa of the genus Theileria cause a babesiosis in this country (Tantaswasdi et al, variety of disease syndromes in domestic and 1998). wild ruminants and other mammals (Bishop Recently, a new type of rodent babesia et al, 2004; Jefferies et al, 2007). Globally, the was detected in Thai bandicoots (Bandicota two most important species that cause indica) using DNA sequence analysis theleriosis in domestic cattle are T. parva and (Dantrakool et al, 2004). This protozoon seems T. annulata (Bishop et al, 2004). Neither of to be phylogenetically most closely related to these two parasites has been reported in Thai- B. canis, the dog parasite, although morpho- land. Nevertheless, benign Theileria that be- logically it looks more like B. microti, a para- long to the Theileria buffeli/orientalis/sergenti site of rodents in North America. Because group, a group of parasites that causes mild Babesia in Thai bandicoot rats is morphologi- disease in cattle (Sarathaphan et al, 1999), and cally pleomorphic, it has been suggested other yet unplaced Theileria parasites (Table there is more than one species. However, the 1), occur in this country. Currently, substan- possibility of multiple infections by different tial research is being conducted regarding species seems quite low because there were the taxonomy of benign Theileria parasites of
Vol 39 No. 6 November 2008 1017 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH ruminants (Gubbels et al, 2000, 2002; Chansiri loes in geographical locations including south- and Sarataphan, 2002; Kim et al, 2004; ern, northern and northeastern Thailand. Mi- Allsopp and Allsopp, 2006), but there is as yet croscopic examination of Giemsa-stained no generally accepted system of classifying blood smears revealed 27.5% of samples were or naming these parasites. Because of this positive for Theileria whereas allele-specific lack of agreement, we report in Table 1 the PCR amplification of the MPSP gene deter- Theileria species found in Thailand by the mined a much higher infection rate of 82.6%. names of the strains and types given them by Among positive cases, the Thai-type of MPSP the researchers. gene was the most common, comprising Two genes, the small subunit ribosomal 67.6% of samples, whereas the C-type com- RNA or ssrRNA gene and the major piroplasm prised only 8.3% of infections. Mixed infections surface protein or MPSP gene, have been were also common with 24% of cases contain- used to investigate genetic relations among ing both MPSP gene types (Sarataphan et al, Theileria isolates in Thailand (Table 1). A third 2003). gene, the thymidylate synthase or TS gene, has Ixodid ticks of the genera Rhipicephalus, also been used by Chansiri and Sarataphan Amblyomma, Hyalomma and Haemaphysalis (2002) to compare the Thai isolate Theileria transmit Theileria parasites (Bishop et al, 2004). sp Thung Song with other Theileria types. No tick species has been identified as a Theile- However, this gene has not been used for ria vector in Thailand, however, three of the four other studies of Thai Theileria parasites and vector genera, namely Rhipicephalus, Amblyo- so we excluded it from Table 1. Three geneti- mma and Haemaphysalis, are represented by cally distinct types of Theileria have been re- more than 30 species in Thailand (Tanskul et corded to occur in Thailand using the MPSP al, 1983); the other genus, Hyalomma, has not gene, ie, types B1, C and Thai (Table 1). The been recorded in this country. Haemaphysalis number of Theileria isolates that are present anomala, Haemaphysalis cornigera, Haema- in Thailand based on the ssrRNA gene is not physalis lagrangei, Haemaphysalis nadchatra- clear, because the two isolates, Thung Song mi, Haemaphysalis bandicota, Haemaphysalis and Thai recorded in Table 1, have not yet heinrichi and Rhipicephalus haemaphysaloides been compared phylogenetically within the are all recorded from Thai domestic cattle same analysis. (Tanskul et al, 1983) and warrant testing for the Theileria parasites have been shown to presence of Theileria parasites. be highly prevalent among Thai domestic ru- Hepatozoon minants. Kaewthamasorn and Wongsamee Hepatozoon parasites cause hepato- (2006) found that 50% of beef cattle (n=162 zoonosis in vertebrates and are transmitted animals tested) in Nan Province, northern Thai- when a vertebrate ingests an invertebrate in- land, were infected with Theileria parasites fected with these parasites (Baneth et al, based on blood characteristics. There were 2003). Transmission has been shown to be no serious observable clinical signs of disease direct, the vertebrate predator directly eats the in any of the positive animals, which suggests Hepatozoon-infected invertebrate prey (Smith, that Theileria infections of beef cattle in this 1996). However, for vertebrates like snakes province are normally not life threatening. for which invertebrates may not be the nor- True infection rates may be underesti- mal prey, an intermediate vertebrate host has mated by hematological analysis. Sarataphan been postulated (Smith, 1996). More than 300 et al (2003) collected a total of 247 blood species of Hepatozoon species are known samples from 214 cattle and 33 water buffa- (Smith, 1996).
1018 Vol 39 No. 6 November 2008 TICK-BORNE PATHOGENS IN THAILAND
Table 1 Molecular detection of tick-borne pathogens in vertebrate hosts in Thailand.
Pathogens Vertebrate hosts References
Protozoaa Babesia bigemina Cattle Jittapalapong et al, 2004 B. canis Dogs Suksawat et al, 2001a,b Babesia sp Bandicota indica (rodent) Dantrakool et al, 2004
Theileria spp classification based on the ssrRNA gene Theileria sp type Thai Cattle Kakuda et al, 1998 Theileria sp type Thung Song Cattle Chansiri et al, 1999
Theileria spp classification based on the MSPS gene Theileria sp type B1 Cattle Sarathaphan et al, 2003 Theileria sp type C Cattle, water buffalo Sarathaphan et al, 1998, 2003 Theileria sp type Thai Cattle, water buffalo Kakuda et al, 1998; Sarathaphan et al, 1998, 2003 Hepatozoon canis Dogs, cats Jittapalapong et al, 2006; Criado-Fornelio et al, 2007b
Rickettsialesb Anaplasma platys Dogs Suksawat et al, 2001a,b; Pinyoowong et al, 2008
Ehrlichia canis Dogs Suksawat et al, 2001a,b; Ariyawutthiphan et al, 2008; Pinyoowong et al, 2008 Rickettsia honei strain TT-118 Humans Jiang et al, 2005 Rickettsia sp strain PMK94 Humans Gaywee et al, 2007
Other bacteriab Bartonella henselae Cats Maruyama et al, 2001 aProtozoa nomenclature: Babesia spp. - Uilenberg (2006); Theileria spp – standard system of classification not available yet in the literature (see text). bNomenclature for Rickettsiales and other bacteria from Kracht (2004).
Like other blood parasites, Hepatozoon Molecular techniques are necessary for infections can be detected by microscopic distinguishing and identifying Hepatozoon examination of blood smears. Hepatozoon in- species. Sequences of the 18S rDNA gene are fections have been found using this method most often used for genetically comparing and in several types of vertebrates in Thailand in- identifying Hepatozoon isolates (Baneth et al, cluding stray and pet dogs (Pukkavesa et al, 2000; Criado-Fornelio et al, 2007a; Allen et 1980; Jittapalapong and Tipsawake 1991; al, 2008). In Thailand, Hepatozoon canis has Jittapalapong et al, 2006; Niwetpathomwat et been identified in stray dogs, pet dogs and al, 2006), stray cats (Jittapalapong et al, 2006), stray cats based on the 18S rDNA gene a species of wild cat (the flat-headed cat, (Jittapalapong et al, 2006; Criado-Fornelio Prionailurus planiceps; Salakij et al, 2008) and et al, 2007b) whereas a yet unnamed species in more than ten snake species (Salakij et al, different to H. canis was found in the flat- 2001, 2002). headed cat (Salakij et al, 2008).
Vol 39 No. 6 November 2008 1019 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH
Table 2 Molecular detection of tick-borne pathogens in ticks in Thailand.
Pathogen Tick speciesc Source References
Protozoaa Babesia bigemina Rhipicephalus (Boophilus) microplus Cattle Jittapalapong et al, 2004
Rickettsialesb Anaplasma platys Dermacentor auratus Dogs Parola et al, 2003a Anaplasma sp strain AnAj360 Amblyomma javanense Pangolin Parola et al, 2003a Anaplasma sp strain AnHl446 Haemaphysalis lagrangei Bear Parola et al, 2003a Ehrlichia sp strain EBm52 Rhipicephalus (Boophilus) microplus Cattle Parola et al, 2003a Rickettsia honei strain TT-118 Ixodes granulatus Rattus rattus Kollars et al, 2001 Rickettsia sp strain SP2464 Ixodes granulatus Rattus rattus Kollars et al, 2001 Rickettsia sp strain RDa420 Dermacentor auratus Bear Parola et al, 2003a Rickettsia sp strain RDla440 Dermacentor sp Pig nest Parola et al, 2003a Rickettsia sp strain ATT Amblyomma testudinarium Vegetation Hirunkanokpun et al, 2003 Rickettsia sp strain HOT1 Hemaphysalis ornithophila Vegetation Hirunkanokpun et al, 2003 Rickettsia sp strain HOT2 Hemaphysalis ornithophila Vegetation Hirunkanokpun et al, 2003 aBabesia nomenclature from Uilenberg (2006). bNomenclature for Rickettsiales and other bacteria from Kracht (2004). cTick nomenclature from Barker and Murrell (2004).
Definitive hosts for Hepatozoon species suggesting that Hepatozoon infections in this consist of a variety of hematophagous inver- part of the world are generally subclinical (Irwin tebrates including ticks, mites, sand flies, and Jefferies, 2004). This contrasts with other tsetse flies, mosquitoes, fleas, lice, reduviid locations where hepatozoonosis can cause bugs, and leeches (Smith, 1996). Ticks have serious illness (Baneth, 2001). been shown to be vectors for Hepatozoon Based on hematological examination, parasites in mammals, birds and lizards estimates of the prevalence of canine (Smith, 1996). In Southeast Asia, H. canis is Hepatozoon infections in stray and pet dogs the major Hepatozoon species known to in- in Thailand are low at 2.6 and 2.2%, respec- fect dogs. Dogs have been shown to become tively (Jittapalapong and Tipsawake, 1991; infected with H. canis after ingesting the brown Jittapalapong et al, 2006). Hepatozoon infec- dog tick, Rhipicephalus sanguineus (Baneth tions have also been detected in stray cats et al, 2001), a species commonly found on but at very low rates (0.7%, Jittapalapong et dogs in many parts of the world, including al, 2006). However, estimates based on mi- Thailand (Tanskul et al, 1983). Hepatozoonosis croscopic examination of blood smears may is a commonly reported illness of Thai dogs underestimate infection rates. Jittapalapong (Pukkavesa et al, 1980; Jittapalapong et al, et al (2006) also determined prevalences 2006; Criado-Fornelio et al, 2007b). In South- based on PCR detection of Hepatozoon canis east Asia, gamonts are only occasionally found and determined infection rates of 11.4 and in the peripheral blood of dogs (as inclusions 32.3%, respectively, in the same samples from in neutrophils and occasionally monocytes), stray dogs and cats that were examined
1020 Vol 39 No. 6 November 2008 TICK-BORNE PATHOGENS IN THAILAND hematologically. discovered, called the Thai tick typhus isolate, The unexpected high prevalence of H. TT-118, was obtained from a mixed pool of canis parasites among stray cats found by Ixodes spp and Rhipicephalus spp larval ticks Jittapalapong et al (2006) indicates that their collected from Rattus rattus trapped in Chiang role in the epizootiology of hepatozoonosis Mai Province in 1962 (Robertson and should be investigated. Both stray dogs and Wisseman, 1973). TT-118 was subsequently cats have potential roles as reservoirs or determined to be a strain of Rickettsia honei, sources of pet infections with H. canis in Thai- the etiologic agent of Flinders Island spotted land. fever in Australia (Stenos et al, 1998). Several documented cases of human patients exhib- RICKETTSIALES iting signs and symptoms of SFG rickettsiosis have been reported in Thailand and in many The Order Rickettsiales is a diverse as- cases their sera were reactive to SFG rickett- semblage of bacterial species, many of which sial antigens. Three patients at a Chiang Mai are associated with ticks. With the advent of hospital showed serological reactions to sev- molecular techniques, genetic relationships eral SFG rickettsias but the tests could not among microbes have become easier to char- confirm which rickettsial species were involved acterize. This is especially so for the Order (Sirisanthana et al, 1994). SFG rickettsias were Rickettsiales, which has undergone extensive also serologically detected in 20 of 46 patients taxonomic revision since genes suitable for presenting with rickettsiosis symptoms at a taxonomic comparison were identified. The hospital on the central Thai-Myanmar border currently accepted classification of Rickett- in western Thailand (Ellis et al, 2006). Further siales and the one used in this review is based serological testing of 8 of these patients on Dumler et al (2001). This order comprises showed antibodies to the SFG rickettsias, R. two families, the Rickettsiaceae and the conorii India, R. helvetica and R. felis (Parola Anaplasmataceae, both of which contain tick- et al, 2003b). Another three patients from borne pathogens. The Rickettsiaceae contain northeastern Thailand were seropositive for R. two genera, Rickettsia and Orientia, of which helvetica (Fournier et al, 2004). Eight (0.9%) only the Rickettsia include tick-borne species. of 854 febrile patients had antibodies to R. The Anaplasmataceae are comprised of four helvetica in a survey that included a total of genera, three of which, Ehrlichia, Anaplasma five hospitals from northeastern, Central and and Neorickettsia, include species carried by southern Thailand (Suttinont et al, 2006). In ticks. The fourth genus, Wolbachia, is wide- the latter survey, R. helvetica antibodies were spread in insects and has been found in sev- detected in patients from both northeastern eral other types of invertebrates but has not and southern but not Central Thailand. been recorded in ticks. Serological surveys in two parts of Thai- Rickettsiaceae land have shown the presence of antibodies Rickettsial infections or rickettsiosis (also to TT-118 to be widespread in communities. called typhus) are a major cause of febrile ill- A survey of 122 farmers in Chiang Rai, north- ness in people throughout the world. Of the ern Thailand, determined that spotted fever two genera comprising the Rickettsiaceae, the antibodies were markedly prevalent (9.0 to Rickettsia include species that are tick-borne 21.3%) with specific reactivity to the TT-118 within a group called the Spotted Fever Group strain occurring in 8.2% of people (Takada or SFG. et al, 1993). In a similar survey in suburban The first Thai member of the SFG to be Bangkok, 4% of 215 people who donated
Vol 39 No. 6 November 2008 1021 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH blood were positive for TT-118 infection sia, R. canadensis, were also found but at a (Strickman et al, 1994). These survey results comparatively lower prevalence (4%) than the along with evidence of infections in hospital other two. The role of the latter Rickettsia in patients suggest that SFG rickettsias are human infection has not been definitely es- widely distributed in various parts of Thailand. tablished (Parola et al, 2005). The first molecular confirmation of a SFG Anaplasmataceae rickettsial infection in a Thai person was pub- Ehrlichiosis is an acute disease that trig- lished by Jiang et al (2005) who used five dif- gers flu-like symptoms in both humans and ferent genes to show the presence of R. honei animals and is caused by infection of para- infection in a patient. Later, Gaywee et al sites that were all previously placed in the ge- (2007) confirmed molecularly the presence of nus Ehrlichia. However, evidence from molecu- DNA of another SFG rickettsia that was very lar phylogenetic analyses using the 16S rRNA similar to R. japonica, the causative agent of gene and groESL operon nucleic acid data and Japanese spotted fever in Japan (Mahara, from serological cross-reactions suggests that 2006) in a patient at a Bangkok hospital. Rick- the genus Ehrlichia should be split into four ettsia have also been determined molecularly genera, which are now designated as in ticks in Thailand (Table 2). Rickettsia honei Ehrlichia, Anaplasma, Neorickettsia and and another undescribed Rickettsia species Wolbachia (Dumler et al, 2001). were detected in the tick, Ixodes granulatus, In the 1970s, substantial epizootic losses whereas two unnamed Rickettsia isolates were of military dogs occurred in Singapore, Thai- found in Dermacentor auratus and unidenti- land, Malaysia and Vietnam (Irwin and fied Dermacentor larvae. In addition, three Jefferies, 2004). The causative agent was de- strains of SFG Rickettsia were detected in termined to be Ehrlichia canis, an obligate in- Amblyomma testudinarium and Hemaphysalis tracellular parasite that infects the host’s ornithophila (Hirunkanokpun et al, 2003). In- monocytes after transmission by Rhipiceph- fection rates in these two tick species were alus sanguineus. Many affected dogs devel- high with 30% of Amblyomma testudinarium oped a rapidly fatal hemorrhagic disease char- and 16.8% of Hemaphysalis ornithophila test- acterized by lethargy, fever, severe epistaxis, ing positive for Rickettsia DNA. Three of the and petechial or ecchymotic hemorrhages. four infected tick species, Ixodes granulatus, The development of terminal bone marrow Dermacentor auratus and Amblyomma suppression, to which German shepherd dogs testudinarium, have been recorded infesting seemed uniquely sensitive, gave rise to the humans (Tanskul et al, 1983). So, these ticks original term “tropical canine pancytopenia” for are potential sources of human rickettsial in- this disease (Irwin and Jefferies, 2004). In Thai- fections in Thailand. land, 161 cases of ehrlichiosis were identified Humans are not the only vertebrates to serologically in a population of 316 military be infected with Rickettsia in Thailand. In a working dogs, of which 54 dogs exhibited study by Suksawat et al (2001a) antigens to clinical or hematological signs of ehrlichiosis three Rickettsia species were detected in Thai (Davidson et al, 1975). Clinical and serologic dogs. The highest prevalence was recorded recognition of ehrlichiosis among pet dogs in for R. prowazekii (24%), the flea-borne agent widely separated regions of Thailand suggests of epidemic typhus. However, the prevalence the disease has been endemic in Thailand for in dogs of antigens to the tick-borne SFG hu- an extended time. Under such circumstances man pathogen R. rickettsii (12%) was also it is possible that pet and stray dogs serve as high. Antigens to another tick-borne Rickett- a source of infection for the epizootic that
1022 Vol 39 No. 6 November 2008 TICK-BORNE PATHOGENS IN THAILAND occurs in Thai military working dogs (Davidson blood of naturally infected cats in Thailand et al, 1975). (Jittapalapong and Jansawan, 1993). The first molecular evidence (Table 1) that Human infections with Ehrlichia were first Anaplasmataceae species infect dogs in Thai- reported in Thailand by Heppner et al (1997) land was provided by Suksawat et al (2001b) who determined about 40% of volunteers in a who confirmed infections by E. canis and A. malaria prophylaxis study from Sangkhla Buri platys. The detection of a supposed third spe- District, Kanchanaburi Province on the Thai- cies, A. phagocytophilum (formerly E. equi), Myanmar border had antibodies to E. by Suksawat et al (2001b) was later deter- chaffeensis, the agent of human monocytic mined to be a PCR artifact (Suksawat et al, ehrlichiosis in the USA. The exact identity of 2002) and so currently there is no molecular the ehrlichial agent reported by Heppner et al evidence for A. phagocytophilum infection in (1997) as E. chaffeensis cannot be determined Thai dogs. Nevertheless, antibodies to A. because of the existence of cross-reactivity phagocytophilum as well as to E. canis, E. among closely-related Ehrlichia species. For chaffeensis and N. risticii have been detected example, cross-reactivity has been reported in dogs that presented to a Bangkok veteri- among E. canis and E. chaffeensis antigens nary teaching hospital with clinical signs of in America (Perez et al, 1996; Kordick et al, ehrlichiosis (Sukswat et al, 2001a). The results 1999). To date, isolates of E. chaffeensis or of this study indicate that dogs in Thailand molecular evidence of infection is limited to have substantial exposure to vector-borne dis- the USA (Suksawat et al, 2001a). eases (Suksawat et al, 2001a). A survey of ticks conducted in the same Several other domestic animals have also part of Thailand where human Ehrlichia infec- been reported to be infected with Anaplas- tion was discovered using PCR to detect bac- mataceae pathogens. In a survey of seven teria of the order Rickettsiales, including those provinces throughout Thailand, up to 74.2% in the family Anaplasmataceae (Parola et al, of calves were determined to be seropositive 2003b). Ticks were collected from peridomestic for A. marginale (Phrikanahok et al, 2000). This and wild animals, from people, or by flagging bacterium is the most prevalent tick-borne the vegetation (Table 2). Three Anaplasma spp pathogen of animals worldwide and is respon- were found, including A. platys, which was sible for severe morbidity and mortality in tem- obtained from Dermacentor auratus ticks col- perate, subtropical, and tropical regions lected from dogs, and two unnamed Ana- (Palmer et al, 2000). The severity of Anaplasma plasma species, one from Amblyomma infection in Thailand was demonstrated in a javanense ticks collected on a pangolin and the case study in Samut Prakan Province, Cen- other from Haemaphysalis lagrangei ticks tral Thailand, in which anaplasmosis was de- collected from a bear. One unnamed Ehrlichia termined to be the cause of death of five of species was determined in Rhipicephalus 30 non-immune cattle (Pemayodhin et al, microplus ticks collected from cattle. Two of 1991). Anaplasma DNA was also found to be these tick species, Dermacentor auratus and common in goats in Satun Province, south- Haemaphysalis lagrangei, have been collected ern Thailand with 16.9% and 6.7% of meat from humans (Tanskul et al, 1983). and dairy goats being infected, respectively In summary, tick-borne parasites of the (Jittapalapong et al, 2005). Cats are normally family Anaplasmataceae confirmed to be considered not to be infected with Ehrlichia present in Thailand include A. platys and E. pathogens. Nevertheless, Ehrlichia-like inclu- canis (Table 1), which can cause severe ca- sions have been detected in the peripheral nine monocytic ehrlichiosis and mild to mod-
Vol 39 No. 6 November 2008 1023 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH erate canine infectious cyclic thrombocytope- (Rodolakis, 2006), and Francisella tularensis, nia in dogs (Irwin and Jefferies, 2004). Of the cause of tularemia in humans and other these, genetic and serological evidence for E. vertebrates (Cunha and Johnson, 2001). canis infection in humans exists (Perez et al, Bartonella species are gram-negative 1996), although not in Thailand. In addition, bacteria that infect erythrocytes, endothelial A. platys and another unnamed Anaplasma cells and macrophages, often leading to per- spp were detected in ticks that sometimes sistent blood-borne infections (Billeter et al, feed on humans. The potential presence in 2008) in mammals including humans (Dehio, Thai dogs of E. chaffeensis supported by se- 2004). Several Bartonella species have been rological evidence is of concern. E. chaffeensis detected in ticks and this evidence along infection has mild effects on dogs (Irwin and with clinical studies in which Bartonella infec- Jefferies, 2004). However, in humans in the tion of animals or humans likely followed tick USA, this parasite can cause severe and even exposure have led to suggestions that ticks fatal human monocytic ehrlichiosis. The ques- may be vectors of these pathogens (Billeter tion concerning whether E. chaffeensis occurs et al, 2008). Nevertheless, no reports have in Thailand or not has not been answered. shown ticks to be Bartonella vectors, whereas However, Ehrlichia strains very closely related several other blood-feeding arthropods, in- to American E. chaffeensis have been found cluding a sandfly (Lutzomyia verrucarum), a in ticks in other countries of the region (South- louse (Pediculus humanus humanus) and two east China-Cao et al, 2000; Japan-Shibata et flea species (Ctenocephalides felis, Cteno- al, 2000; Vietnam-Parola, et al, 2003b). These phthalmus nobilis nobilis), have been con- findings highlight the potential for novel ana- firmed as vectors (Billeter et al, 2008). Of the plasmoses and ehrlichioses to develop in Thai- Bartonella species with serological or molecu- land as well as the need for accurate diag- lar evidence of occurrence in mammals in nostic tools for determining the identities of Thailand (see below), only B. henselae and B. tick-borne pathogens in this country. vinsonii ssp berkhofii are known from ticks in other parts of the world (Billeter et al, 2008) OTHER BACTERIAL PATHOGENS but not Thailand. Evidence of Bartonella presence in Thai- Several types of bacterial pathogens land has been provided by several studies that other than rickettsial bacteria are often car- have shown infection in various mammal spe- ried by ticks. They include Bartonella spp cies. Blood samples of cats and dogs that which cause bartonellosis, a disease associ- presented to an animal teaching hospital in ated with a variety of clinical syndromes in Bangkok were found to have antibodies to B. humans, the best known of which is cat henselae and B. vinsonii ssp berkhofii, respec- scratch disease (Irwin and Jefferies, 2004) and tively (Boonmar et al, 1997; Suksawat et al, which may also be responsible for several 2001a). Molecular techniques have detected conditions in cats and dogs (Breitschwerdt et several Bartonella strains in three species of al, 1999; Shaw et al, 2001b), Borrelia spp, rodents (Bandicota indica, Rattus losea and which cause lyme disease and relapsing fe- Rattus rattus) in Chiang Rai Province, north- ver in humans (Parola and Raoult, 2001; ern Thailand (Castle et al, 2004) as well as Rebaudet and Parola, 2006), Coxiella burnetii, determined B. clarridgeiae and B. henselae to which causes Q fever throughout the world be present in 27.6% of cats throughout Thai- and infects arthropods, birds, pets, domestic land (Maruyama et al, 2001). A Bartonella and wild mammals, as well as humans strain detected in the blood of three human
1024 Vol 39 No. 6 November 2008 TICK-BORNE PATHOGENS IN THAILAND patients from Khon Kaen Province in north- have been no published reports of tularemia eastern Thailand has been proposed as a new or Francisella infections in Thailand. However, Bartonella species, B. tamiae (Kosoy et al, a warning of tularemia has been posted re- 2008). cently by the Thailand’s Department of Dis- Borrelia species causing lyme disease ease Control (MCOT enews, 2008). Hirun- and relapsing fever are not known to be in kanokpun et al (2003) tested 14 tick species Thailand or elsewhere in Southeast Asia for several pathogens including Francisella (Rebaudet and Parola, 2006). Borrelia species but the results were negative for Francisella that cause lyme disease are transmitted by DNA. Ixodes ticks and those that cause relapsing Coxiella burnetii, the agent for Q-fever, fever are transmitted by Ornithodoros ticks. can infect a broad spectrum of susceptible Both tick genera are represented by several hosts including domestic animals (livestock species in Thailand (Tanskul et al, 1983). How- and pets), wildlife and even non-mammalian ever, none of the tick species recorded as species including reptiles, fish, birds and ticks Borrelia vectors in other parts of the world are (Cutler et al, 2007). Human infection is usu- known in Thailand (Tanskul et al, 1983; Parola ally via shedding of C. burnetii in milk, feces, and Raoult, 2001). Hirunkanokpun et al (2003) urine and birth products from infected rumi- examined ticks for several human pathogens, nants. Infection is mainly acquired through in- including Borrelia. They were unable to detect halation of infectious aerosols, at parturition Borrelia DNA in 334 ticks representing 14 spe- (including normal births) or at slaughter. In cies tested. However, none of the species humans, infection is often asymptomatic, and tested by Hirunkanokpun et al (2003) were in in its mild form can be mistaken for other flu- the genera Ixodes or Ornithodoros. like illnesses. It can, however, be associated Tularemia in humans and animals is with chronic or even fatal infections, usually caused by F. tularensis, a small gram-nega- endocarditis. Though this organism is endemic tive intracellular bacterium (Parola and Raoult, in the environment, infection is rarely reported. 2001). It seems to be a disease of temperate Ticks can be infected with C. burnetii. Their zones of the Northern Hemisphere (Cunha significance for causing human disease has and Johnson, 2001). The pathogen is trans- yet to be established (Cutler et al, 2007). Cox- mitted to humans by bites from infected ar- iella burnetii infection in humans has been re- thropod vectors with the primary vectors be- ported in Thailand. Supattamongkol et al ing ticks and deer flies, as well as by various (2003) reported C. burnetii to be present in 9 other routes, including the direct handling of of 678 (1.3%) febrile patients in northeastern infectious carcasses, the ingestion of con- Thailand based on serological tests. In another taminated food, vegetation or water, and the serological study, one positive case in 133 was inhalation of infectious dust, soil or aerosols detected in febrile patients in a hospital near (Ellis et al, 2002). Domestic and wild animal the Thai-Myanmar border in Kanchanaburi population movements may be important in (Ellis et al, 2006). The authors considered the the spread of diseases like tularemia. In a single positive case to be insufficient evidence recent case, potentially Francisella-infected for the presence of C. burnetii in the area. Their prairie dogs were distributed to wholesalers, conclusion is supported by another survey of retailers, and persons worldwide, including febrile patients at the same hospital conducted Thailand (Avashia et al, 2004). Despite the using molecular markers in which no cases of potential for spread of Francisella in Thailand C. burnetii infection were found (Parola et al, through importation of infected animals, there 2003a).
Vol 39 No. 6 November 2008 1025 SOUTHEAST ASIAN J TROP MED PUBLIC HEALTH
FLAVIVIRAL PATHOGENS widely distributed in Thailand (Tanskul et al, 1983) and this suggests that the virus may be The mammalian tick-borne flavivirus com- present in other areas of the country (Bancroft plex includes Kyasanur forest disease, Langat, et al, 1976). Both tick species have been re- Louping ill, Negishi, Omsk hemorrhagic fever, corded on humans (Tanskul et al, 1983) and Powassan, and tick-borne encephalitis viruses may potentially transmit Langat virus to hu- (Labuda and Nuttall, 2004). Of these, only mans. Langat virus has been found in Thailand. The vector-competent hosts of these viruses are CONCLUSION ticks belonging to the family Ixodidae (hard ticks). The most serious of these viruses is the Ticks and pathogens borne by ticks are tick-borne encephalitis virus, which is distrib- common in urban, rural and forest environ- uted from northern Europe through Siberia to ments in Thailand. Hematological and sero- northern Asia (Labuda and Nuttall, 2004). No logical evidence indicates that such pathogens cases of tick-borne encephalitis have been can infect and cause severe disease in hu- reported in Southeast Asia. mans and domestic animals. However, these Langat virus (isolate TP21) was originally techniques often do not allow the identifica- isolated in the 1950s from a pool of Ixodes tion of pathogens to species level. In recent granulatus ticks from forest rats caught in years, however, the advent of molecular tech- Malaysia (Smith, 1956). Antibodies to Langat- niques has resulted in accurate identification TP21 were detected in sera of 6 of 51 forest of tick-borne pathogens and diagnosis of the rats. Some human sera that had antibodies diseases they cause. In particular, the use of to Langat-TP21 also had antibodies to Japa- techniques such as multiplex and real-time nese encephalitis virus, but this was consid- quantitative PCR can greatly enhance our un- ered to indicate cross-reactivity between the derstanding of the epidemiology of tick-borne two viruses and not conclusive evidence of diseases in Thailand. human infection with Langat virus (Smith, Large numbers of infected stray cats and 1956). Langat virus is the only representative dogs roam streets, fresh open markets, and of the tick-borne flavivirus group that has not other public places in Thailand’s urban areas. been found to cause human disease in natu- These stray cats and dogs may act as sources ral foci (Il’enko et al, 1968). Recently, antibod- of tick-borne zoonotic diseases (Jittapalapong ies to Langat virus were detected in the sera et al, 2006). Companion animals seem most of one human (114 tested) and one orangu- at risk for contracting tick-borne diseases from tan (71 tested) in Malaysia (Wolfe et al, 2001). these stray animals (Irwin and Jefferies, 2004). However, it is difficult to form conclusions on Nevertheless, experimental evidence that con- the basis of one positive result for each pri- clusively demonstrates the roles and relative mate species. In Thailand, a strain of Langat importances of stray dog and cat populations virus (isolate T-1674), was isolated from a pool as well as the feral rodent populations in in- of Haemaphysalis papuana ticks collected fecting companion animals is lacking but is from vegetation in Khao Yai National Park needed in Thailand. (Bancroft et al, 1976). No antibodies were In Thailand’s rural and forest areas, dif- found in any of 190 Rattus or other small mam- ferent ticks and tick-borne diseases exist. mals sampled in the same area. Livestock, particularly cattle, are at risk for se- Both Langat virus carrier ticks, Ixodes vere disease and even death caused by tick granulatus and Haemaphysalis papuana, are borne Babesia and Anaplasma species that
1026 Vol 39 No. 6 November 2008 TICK-BORNE PATHOGENS IN THAILAND may result in substantial losses to rural liveli- REFERENCES hoods. Despite these diseases’ severity, little Allen KE, Li Y, Kaltenboeck B, et al. Diversity of is known of the extent of each disease-caus- Hepatozoon species in naturally infected dogs ing pathogen species throughout Thailand. in the southern United States. Vet Parasitol The risk factors associated with each bovine 2008; 154: 220-5. tick-borne disease have not been character- Allsopp MTEP, Allsopp BA. Molecular sequence ized. Better management and therefore evidence for the reclassification of some Ba- greater relief for cattle and other livestock besia species. Ann NY Acad Sci 2006; 1081: owners can only come about from better un- 509-17. derstanding of these diseases. Finally, live- Ariyawutthiphan O, Shokshai-utsaha K, Sananmuang stock, wildlife and animal products imported T, Chungpivat S, Sarikaputi M, Viseshakul N. into Thailand should be carefully monitored for The microscopic and molecular detections of tick-borne and other diseases. canine ehrlichiosis. Thai J Vet Med 2008; 38: 29- Rickettsioses and perhaps babesioses 36. may be a hazard to humans who work or Avashia SB, Petersen JM, Lindley CM, et al. First re- spend their leisure time in Thailand’s rural and ported prairie dog-to-human tularemia trans- forest areas. People such as forest workers mission, Texas, 2002. Emerg Infect Dis 2004; and ecotourists who spend time in dense 10: 483-6. vegetation, especially in the high tick season, Bancroft WH, M Scott RM, Snitbhan R, Weaver RE, are at greatest risk. Very little is known of the Jr, Gould DJ. Isolation of Langat virus from pathogens carried by ticks in these areas or Haemaphysalis papuana Thorell in Thailand. Am J Trop Med Hyg 1976; 25: 500-4. of their vertebrate reservoir hosts. Yet, as re- forestation programs continue in this coun- Baneth G, Barta JR, Shkap V, Martin DS, Macintire DK, Vincent-Johnson N. Genetic and antigenic try and increasing numbers of tourists visit evidence supports the separation of Thailand’s national parks, it can be expected Hepatozoon canis and Hepatozoon that many more people will contract tick- americanum at the species level. J Clin borne diseases. Knowing what tick-borne Microbiol 2000; 38: 1298-301. pathogens are present and the tick species Baneth G, Samish M, Alekseev E, Aroch I, Shkap V. and vertebrate hosts that carry them in these Transmission of Hepatozoon canis to dogs by areas may help in the rapid diagnosis of novel naturally-fed or percutaneously-injected Rhipi- diseases that present in people who visit cephalus sanguineus ticks. J Parasitol 2001; these areas. 87: 606-11. Baneth G, Mathew JS, Shkap V, Macintire DK, Barta ACKNOWLEDGEMENTS JR, Ewing SA. Canine hepatozoonosis: Two disease syndromes caused by separate The authors thank Dr Libor Grubhoffer Hepatozoon spp. Trends Parasitol 2003; 19:
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