Review. Tick-Borne Pathogens and Diseases of Animals and Humans In
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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.