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    Provincial map of Thailand showing the eight provinces in which rodents were collected.

  • 1

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    Walker JS, Chan CT, Manikumaran C, Elisberg BL, 1975. Attempts to infect and demonstrate transovarial transmission of R. tsutsugamushi in three species of Leptotrombidium mites.Ann NY Acad Sci 266: 80–90.

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    Takahashi M, Murata M, Misumi H, Hori E, Kawamura A Jr, Tanaka H, 1994. Failed vertical transmission of Rickettsia tsutsugamushi (Rickettsiales: Rickettsiaceae) acquired from rickettsemic mice by Leptotrombidium pallidum (Acari: Trombiculidae). J Med Entomol 31 :212–216.

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    Frances SP, Watcharapichat P, Phulsuksombati D, Tanskul P, 2000. Transmission of Orientia tsutsugamushi, the aetiological agent for scrub typhus, to co-feeding mites. Parasitology 120 :601–607.

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    Takahashi M, Murata M, Hori E, Tanaka H, Kawamura A Jr, 1990. Transmission of Rickettsia tsutsugamushi from Apodemus speciosus, a wild rodent, to larval trombiculid mites during the feeding process. Jpn J Exp Med 60 :203–208.

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    Traub R, Wisseman CL Jr, Jones MR, O’Keefe JJ, 1975. The acquisition of Rickettsia tsutsugamushi by chiggers (trombiculid mites) during the feeding process. Ann NY Acad Sci 266 :91–114.

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    Frances SP, Watcharapichat P, Phulsuksombati D, Tanskul P, Linthicum KJ, 1999. Seasonal occurrence of Leptotrombidium deliense (Acari: Trombiculidae) attached to sentinel rodents in an orchard near Bangkok, Thailand. J Med Entomol 36 :869–874.

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  • 14

    Tanskul P, Strickman D, Eamsila C, Kelly DJ, 1994. Rickettsia tsutsugamushi in chiggers (Acari: Trombiculidae) associated with rodents in central Thailand. J Med Entomol 31 :225–230.

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    Philip RN, 1980. Scrub typhus. Steele JH, ed. CRC Handbook Series in Zoonoses, Section A: Bacterial, Rickettsial and Mycotic Diseases. Volume II. Boca Raton, FL: CRC Press, 303–315.

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    Urakami H, Tamura A, Tarasevich IV, Kadosaka T, Shubin FN, 1999. Decreased prevalence of Orientia tsutsugamushi in trombiculid mites and wild rodents in the Primorye region, Far East Russia. Microbiol Immunol 43 :975–978.

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    Frances SP, Watcharapichat P, Phulsuksombati D, Tanskul P, 1999. Occurrence of Orientia tsutsugamushi in chiggers (Acari: Trombiculidae) and small animals in an orchard near Bangkok, Thailand. J Med Entomol 36 :449–453.

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    Ree HI, Cho MK, Lee IY, Jeon SH, 1995. Comparative epidemiological studies on vector/reservoir animals of tsutsugamushi disease between high and low endemic areas in Korea. Korean J Parasitol 33: 27–36.

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    Tanskul P, Linthicum KJ, 1999. Redescription of Leptotrombidium (Leptotrombidium) imphalum (Acari: Trombiculidae), with observations on bionomics and medical importance in northern Thailand. J Med Entomol 36 :88–91.

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  • 21

    Tanskul P, Linthicum KJ, 1997. A new species of Leptotrombidium (Acari: Trombiculidae), collected in active rice fields in northern Thailand. J Med Entomol 34 :368–371.

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  • 22

    Roberts LW, Robinson DM, Rapmund G, Walker JS, Gan E, Ram S, 1975. Distribution of Rickettsia tsutsugamushi in organs of Leptotrombidium (Leptotrombidium) fletcheri (Prostigmata: Trombiculidae). J Med Entomol 12 :345–348.

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    Strickman D, Smith CD, Corcoran KD, Ngampochjana M, Watcharapichat P, Phulsuksombati D, Tanskul P, Dasch GA, Kelly DJ, 1994. Pathology of Rickettsia tsutsugamushi infection in Bandicota savilei, a natural host in Thailand. Am J Trop Med Hyg 51: 416–423.

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    Van Peenen PFD, Ho CM, Bourgeois AL, 1977. Indirect immunofluorescence antibodies in natural and acquired Rickettsia tsutsugamushi infections of Phillippine rodents. Infect Immun 15 :813–816.

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  • 26

    Frances SP, Watcharapichat P, Phulsuksombati D, 2000. Development and persistence of antibodies to Orientia tsutsugamushi in the roof rat, Rattus rattus and laboratory mice following attachment of naturally infected Leptotrombidium deliense.Acta Trop 77 :279–285.

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OCCURRENCE OF ORIENTIA TSUTSUGAMUSHI IN SMALL MAMMALS FROM THAILAND

Extensive sampling of small mammals was conducted in eight provinces of Thailand between September 9, 1992 and April 29, 2001. A total of 3,498 specimens representing 22 species were collected. Eighty-eight percent (3,089 of 3,498) of the animals were collected from a region in Chiangrai Province, which is commonly recognized as endemic for human scrub typhus. Blood and tissue samples from each animal were tested for the presence of Orientia tsutsugamushi, the etiologic agent of scrub typhus. The predominant species collected were Rattus rattus (53%, n = 1,863), R. losea (18%, n = 638), Bandicota indica (16%, n = 564), and R. exulans (4%, n = 146). Orientia tsutsugamushi was detected in 10 of the 22 species of mammals that included R. bukit (25% infected, 1 of 4), R. rattus (23%, 419 of 1,855), R. argentiventer (22%, 5 of 23), R. berdmorei (22%, 2 of 9), R. losea (13%, 82 of 638), B. indica (9%, 52 of 564), R. koratensis (8%, 1 of 12), B. savilei (3%, 1 of 30), R. exulans (1%, 2 of 146), and Tupaia glis (2%, 1 of 49). Infected animals were found in Chiangrai (18% infected, 563 of 3,084), Bangkok (11%, 1 of 9), Sukothai (3%, 1 of 30), and Nonthaburi (1%, 1 of 69) Provinces. The implications towards scrub typhus maintenance and transmission are discussed.

INTRODUCTION

Scrub typhus is an acute febrile zoonotic disease resulting from infection with the gram-negative, intracellular bacteria Orientia (formerly Rickettsia) tsutsugamushi (Hyashi).1,2 The disease occurs widely in the Palaearctic, Oriental, and Australasian regions, including southeast Asia where it can account for 10–19% of patients admitted to hospitals with acute pyrexia of uncertain origin.3,4 Approximately one million cases occur each year and more than a billion people are at risk worldwide.2,5 Clinical manifestations of scrub typhus range from mild fever with few other symptoms to a fatal syndrome characterized by multiple-organ failure. The treatment of choice is doxycycline, but other tetracycline antibiotics and chloramphenicol are commonly used for effective and rapid cure.6

Scrub typhus is transmitted by several species of larval trombiculid mites, which are commonly known as chiggers.7 Chiggers are unique among vectors in that they are parasitic in only one stage (i.e., as larvae) and normally attach to and feed upon only a single vertebrate and therefore cannot acquire an infection from one host and subsequently transmit it to a second host.12 Transovarial transmission is thought to be the only mechanism for maintenance of O. tsutsugamushi in the vector.8,9 Infected chiggers can therefore be considered the true hosts of O. tsutsugamushi, and even commonly infected mammals are dead-end hosts rather than true reservoirs. Frances and others10 demonstrated that O. tsutsugamushi could be transmitted to co-feeding mites, and Takahashi and others11 were able to infect chiggers fed on wild rodents; however, neither study determined if infected mites transmitted the rickettsiae to their eggs. Traub and others12 were the first to document horizontal transmission of O. tsustsugamushi, although even this report discussed the possibility that the observation was not representative of natural transmission. In Thailand, Leptotrombidium deliense is the primary vector of scrub typhus;13 however, several other species have been implicated as vectors and include L. chiangraiensis,7 L. imphalum,7 and Blankaartia acuscutellaris.14

Although rodents may not be the true reservoir of O. tsutsugamushi,15 they are critical to the maintenance of the disease. Rodents serve as hosts for chiggers, and chigger distribution often directly reflects the distribution of the rodent host. Foci of infection termed typhus islands have been reported in some areas and described as sharply localized and irregularly scattered areas where transmission is common.16 The sizes of these foci are determined by the range of vector mites and their maintaining hosts.

Evaluation of vertebrates for infection with O. tsutsugamushi and for the presence of vector mites can provide key information on the focality of scrub typhus.17–19 In this study, we report O. tsutsugamushi infection rates and chigger infestation rates from small mammals collected from a number of locations throughout Thailand. Primary emphasis was placed on collecting mammals from a region endemic for scrub typhus in Chiangrai Province in northern Thailand.

MATERIALS AND METHODS

Small mammal and chigger collection.

All procedures involving animals were conducted under animal use protocols approved by the Armed Forces Research Institute of Medical Sciences Institutional Animal Care and Use Committee. Small mammals were routinely collected during studies on the epidemiology of scrub typhus in Chiangrai,7,20,21 Nonthaburi,18 and Phitsanulok21 Provinces of Thailand. Collections in additional provinces were made on an irregular basis. The location of provinces in which collections were made is shown in Figure 1. The collections reported in this study were made between September 9, 1992 and April 29, 2001. Mammals were captured by hand or in live-capture traps baited with bananas or dried fish, anesthetized with pentobarbitol, identified to species, and examined under a dissecting microscope for chiggers. Following examination, tissue (blood, spleen, and liver) specimens were collected and frozen in dry ice. Animals were then humanely killed with carbon dioxide. Chiggers removed from the host were counted and placed alive in vials moistened with tap water. Chiggers transported in these vials survived several days during transport back to the laboratory in Bangkok. The engorged chiggers were reared to adults, providing specimens that could be identified without preservation or slide-mounting.

This research was conducted in compliance with the Animal Welfare Act and other Federal statutes and regulations relating to animals and experiments involving animals and adheres to principles stated in the Guide for the Care and Use of Laboratory Animals, NRC Publication, 1996 edition.

Isolation of O. tsutsugamushi.

Isolation of O. tsutsugamushi in the laboratory was attempted by inoculation in ICR mice. Tissues harvested from the field-collected mammals were triturated in Ten Broeck tissue grinders (Labglass, Vineland, NJ) in 1.5 mL of Snyder’s I tissue culture medium.7 Approximately 0.2 mL of tissue suspension was inoculated intraperitoneally into three adult mice. A veterinarian observed the mice for 30 days for of O. tsutsugamushi infection (rough coat, inactivity, inappetance). Mice judged to be ill were humanely killed to harvest peritoneal scrapings. The scrapings were examined microscopically for the presence of O. tsutsugamushi using both staining with Giemsa and the direct immunofluorescence assay22 to visualize rickettsial particles. Mice that did not develop clinical scrub typhus at the end of the 30-day observation period were humanely killed and their sera were assayed for antibody against O. tsutsugamushi using the indirect immunoperoxidase test.7 This procedure was used to ascertain that mice did not develop subclinical infections.

Statistical analysis.

Analysis of variance with Tukey’s mean separation procedures (P < 0.05) was used to determine if chigger infestation rates varied among three species of rodents collected in three villages in northern Thailand. Pearson’s correlation was used to examine relationships between 1) the percentage of animals infested with chiggers and animal infection rates, and 2) the mean number of chiggers infesting a given species and O. tsutsugamushi infection rates in that species.

RESULTS

A total of 3,498 small mammals representing 22 species in six families were collected over the course of the study (Table 1). The predominant species collected were Rattus rattus (53%, n = 1,863), R. losea (18%, n = 638), Bandicota indica (16%, n = 564), and R. exulans (4%, n = 146). Seventy-eight percent (2,711) of the animals were adults and 58% (2,045) were female. Eighty-eight percent (3,089) of the animals were collected in Chiangrai Province, 7% (242) in Kanchanaburi Province, 2% (69) in Nonthaburi Province, 1% (45) in Phitsanulock Province, 1% (30) in Sukhothai Province, and 1% (23) in Bangkok, Khorat, and Uttradit Provinces.

Approximately 93% (3,240) of animals were checked for ectoparasites (Table 2). A total of 2,587 (80%) animals were infested with one or more chiggers, with a total of 153,899 chiggers collected from these animals. The greatest densities of chiggers were found on R. koratensis (mean of 142/animal), Tupaia glis (112), R. argentiventer (78), R. surifer (58), B. indica (57), R. rattus (54), and Menetes berdmorei (53). Sixty-six percent (102,046) of the chiggers were identified to genus and/or species (Table 3). Leptotrombidium imphalum (62,645) and L. chiangraiensis (6,701) accounted for 45% of the total collection. Approximately 21% (31,845) and < 1% (1,215) of chiggers were in the genera Ascoschoengastia and Blankaartia. The distribution of the different genera and/or species of chiggers on the different species of mammals is shown in Table 3.

Orientia tsutsugamushi was isolated from 16% (566) of the 3,498 small mammals tested (Table 4). Orientia tsutsugamushi was detected in 10 of the 22 species of mammals tested, with 98% (553) of infections found in B. indica (52), R. losea (82), and R. rattus (419). High O. tsutsugamushi infection rates (>20%) were found in R. rattus, R. bukit, R. berdmorei, and R. argentiventer; however, only R. rattus was collected in high numbers (Table 4). Overall, a significantly higher proportion of sub-adults (21%; 166 of 786) were infected with O. tsutsugamushi than adults (15%, 400 of 2,712). Rattus rattus was the only animal species with higher O. tsutsugamushi infection rates in the sub-adult population than in the adult population (Table 4). None of the laboratory mice that failed to develop clinical symptoms of scrub typhus following inoculation with tissue samples from the field-collected animals was positive by the indirect immunoperoxidase test. These data suggested that this method was effective for detecting O. tsutsugamushi.

Eighty-four percent (2,951 of 3,498) of all rodents evaluated in this study were B. indica, R. losea, or R. rattus that had been collected in the villages of MaeSad, PaGook, and Nongrouk in Chiangrai Province (Table 5). For all three species of rodent, O. tsutsugamushi infection rates were highest in PaGook village and lowest in MaeSad village. There were no differences in the number of chiggers found on B. indica in any of the three villages, with a mean ± SEM of 54.4 ± 3.9 chiggers/animal. Fewer chiggers were found on the infected animals than on the uninfected animals (Table 5). A mean ± SEM of 25.4 ± 1.4 chiggers were found on all R. losea. Significantly more chiggers were found on the R. losea collected in Nongrouk village than in PaGook or MaeSad villages. More chiggers were found on infected R. losea collected in MaeSad and PaGook villages compared with uninfected R. losea, whereas, more chiggers were found on uninfected R. losea collected in Nongrouk village (Table 4). A mean ± SEM of 50.1 ± 1.6 chiggers were found on all R. rattus. Significantly more chiggers were found on R. rattus collected in Nongrouk village than in either MaeSad or PaGook villages. Although R. rattus in PaGook village had higher O. tsutsugamushi infection rates compared with the other villages, R. rattus in PaGook were infested with significantly fewer chiggers than animals in either of the other villages. In contrast, uninfected R. rattus collected in Nongrouk village had significantly more chiggers than did uninfected R. rattus collected in either MaeSad or PaGook villages.

DISCUSSION

The role of mammals as reservoirs of O. tsutsugamushi remains a controversial topic. Although studies by Traub and others,12 Walker and others,8 Takahashi and others,11 and Frances and others10 have demonstrated that chiggers can acquire O. tsutsugamushi during the feeding process, to date mammals have not been shown to play a conclusive role in the cyclical transmission of this pathogen.13 In spite of this, rodents play a key role in the epidemiology of scrub typhus, as rodents serve as maintenance hosts for the vector mites.15

Although a total of 22 species were collected in this study, only R. rattus (53%, 1,855 of 3,485), R. losea (18%, 638 of 3,485), B. indica (16%, 564 of 3,485), and R. exulans (4%, 146 of 3,485) were collected in significant numbers (Table 1). The dominance of these species could have been due to the trapping method or the trap placement, rather than the absolute abundance of the species in each area. Certainly, the genus Rattus probably dominates the rodent fauna in the areas of northern Thailand sampled.

More significantly, only R. rattus, R. losea, and B. indica were commonly infected with O. tsutsugamushi (Table 4). Ninety-eight percent (553 of 565) of infected mammals belonged to these three species. There was no significant correlation between the percentage of animals of a given species infested with chiggers and O. tsutsugamushi infection rates (r2 = 0.16), nor was there a correlation between the mean number of chiggers per individual of a given species and O. tsutsugamushi infection rates (r2 = 0.02). Although we did not determine chigger infection rates, these data suggest that infection rates in the different species of mammals may be independent of chigger densities. Strickman and others23 reported that B. savilei mounts a vigorous immune response that limits the infection in this species to no more than 2–3 weeks. In contrast, many Rattus species maintain O. tsutsugamushi infections for months or longer.12,24,25 For example, O. tsutsugamushi was isolated up to eight weeks after attachment of a single infected L. deliense larva on R. rattus.26 Differences in infection rates among the different species of mammals could reflect differences in the course of infection as observed by Strickman and others23 with B. savilei. Alternatively, the site at which the mammals were collected could affect infection rates. The Armed Forces Research Institute of Medical Sciences AFRIMS has maintained a long-term scrub typhus study site in Chiangrai Province in northern Thailand. Historically, high O. tsutsugamushi infection rates have been found in chiggers, rodents, and humans from this area.5,7,20,21 In this study, infected mammals were found in only four (Chiangrai, Bangkok, Nonthaburi, and Sukothai) of eight provinces; however, 99.6% (563 of 565) of infected mammals were found in Chiangrai Province, with only a single infected animal found in Bangkok, Nonthaburi, and Sukothai Provinces. Certain species of animals with low O. tsutsugamushi infection rates were rarely found in Chiangrai Province. For example, only 7% (2 of 30) of B. savilei and 11% (1 of 9) of R. bowersi were collected in Chiangrai Province. Low infection rates in these species may reflect differences in infection rates in different regions of Thailand, rather than any inherent differences in host susceptibility to O. tsutsugamushi.

The question of whether a particular species of rodent is important in maintaining a scrub typhus focus has practical significance in this age of ever increasing world trade and transportation. Introduction of the right species of rodent with its associated chiggers could conceivably start a focus of scrub typhus in a new area. Experimental studies with species of rodents most likely to get exported to other parts of the world (e.g., R. exulans, R. losea) might be the most appropriate means of determining whether their invasion of new areas would expand the range of scrub typhus.

Table 1

Summary of small mammals collected between 1992 and 2001 in Thailand

Total number of animals collected
AdultsSub-Adults
FemaleMaleFemaleMaleTotal
Order Scandentia, Family Tupaiidae (treeshrews)
    Tupaia glis292049
Order Insectivora, Family Soricidae (shrews)
    Crocidura dracula11
    Crocidura horsfieldi10313
Order Rodentia, Family Sciuridae (squirrels)
    Menetes berdmorei17724
Order Rodentia, Family Muridae (rats and mice)
    Bandicota indica22613012880564
    Bandicota savilei1773330
    Mus caroli44186169
    Mus cervicolor113317
    Rattus argentiventer983323
    Rattus berdmorei639
    Rattus bowersi639
    Rattus bukit224
    Rattus exulans845381146
    Rattus koratensis56112
    Rattus losea2482846442638
    Rattus nitidus11
    Rattus norvegicus22
    Rattus rattus8156082821581,863
    Rattus sabanus11
    Rattus surifer14519
Order Carnivora, Family Mustelidae (weasels and otters)
    Melogale personata11
Order Carnivora, Family Viverridae (civets and Mongooses)
    Herpestes javanicus1113
    Total1,5491,1624962913,498
Table 2

Chiggers removed from 16 species of small mammals collected between 1992 and 2001 in Thailand

Host speciesNo. of animals infestedNo. of animals examined% infestedTotal no. of chiggers collectedMean no. of chiggers per animal (SEM)
Bandicota indica40055771.831,58156.7 (4.3)
Bandicota savilei253083.31,33244.4 (6.7)
Crocidura horsfieldi31323.1352.7 (1.5)
Menetes berdmorei91275.063653.0 (19.4)
Mus caroli335263.593918.1 (3.5)
Mus cervicolor61735.322613.3 (6.8)
Rattus argentiventer212391.31,79578.0 (16.5)
Rattus berdmorei2366.77023.3 (14.5)
Rattus bowersi11100.02727.0 (–)
Rattus bukit3475.0143.5 (2.3)
Rattus exulans336154.15829.5 (2.3)
Rattus koratensis1212100.01,709142.4 (28.7)
Rattus losea52263881.816,30925.6 (1.4)
Rattus rattus1,4991,78184.295,89653.8 (1.7)
Rattus surifer77100.040658.0 (20.6)
Tupaia glis112152.42,342111.5 (41.5)
    Total2,5873,24079.8153,89947.5 (1.3)
Table 3

Species of chiggers removed from 16 species of small mammals collected between 1992 and 2001 in Thailand

No. of chiggers collected (% of total in row)
Host speciesLeptotrombidium chiangraiensisLeptotrombidium imphalumBlankaartia sps.Ascoschoengastia sps.Not identifiedTotal collected
Bandicota indica111 (<1)14,802 (47)881 (3)8,592 (27)7,404 (23)31,790
Bandicota savilei352 (26)10 (<1)583 (44)387 (29)1,332
Crocidura horsfieldi20 (57)15 (43)35
Menetes berdmorei293 (46)159 (25)184 (29)636
Mus caroli30 (3)150 (16)120 (13)633 (67)6 (<1)939
Mus cervicolor1 (<1)225 (9)226
Rattus argentiventer888 (49)75 (4)832 (46)1,795
Rattus berdmorei20 (29)50 (71)70
Rattus bowersi27 (100)27
Rattus bukit1 (7)3 (21)10 (71)14
Rattus exulans67 (12)454 (78)61 (10)582
Rattus koratensis1,423 (83)31 (2)255 (15)1,709
Rattus losea1,537 (9)4,351 (27)46 (<1)6,712 (41)3,691 (23)16,337
Rattus rattus5,023 (5)37,905 (40)158 (<1)13,855 (14)38,718 (40)95,659
Rattus surifer100 (25)96 (24)210 (52)406
Tupaia glis2,272 (97)40 (2)30 (1)2,342
    Total6,701 (4)62,645 (41)1,215 (<1)31,485 (20)51,853 (34)153,899
Table 4

Infection of 22 species of mammals with Orientia tsutsugamushi, the causative agent of scrub typhus

No. of animals infected with O. tsutsugamushi/no. tested (% positive)
AdultsSub-adults
FemaleMaleFemaleMaleTotal
Bandicota indica17/226 (8)10/130 (8)15/128 (12)10/80 (13)52/564 (9)
Bandicota savilei0/17 (0)0/7 (0)1/3 (33)0/3 (0)1/30 (3)
Crocidura dracula0/1 (0)0/1 (0)
Crocidura horsfieldi0/10 (0)0/3 (0)0/13 (0)
Herpestes javanicus0/1 (0)0/1 (0)0/1 (0)0/3 (0)
Melogale personata0/1 (0)0/1 (0)
Menetes berdmorei0/17 (0)0/7 (0)0/24 (0)
Mus caroli0/44 (0)0/18 (0)0/6 (0)0/1 (0)0/69 (0)
Mus cervicolor0/11 (0)0/3 (0)0/3 (0)0/17 (0)
Rattus argentiventer2/9 (22)1/8 (13)1/3 (33)1/3 (33)5/23 (22)
Rattus berdmorei2/6 (33)0/3 (0)2/9 (22)
Rattus bowersi0/6 (0)0/3 (0)0/9 (0)
Rattus bukit½ (50)0/2 (0)¼ (25)
Rattus exulans0/84 (0)2/53 (4)0/8 (0)0/1 (0)2/146 (1)
Rattus koratensis0/5 (0)1/6 (17)0/1 (0)1/12 (8)
Rattus losea32/248 (13)37/284 (13)7/64 (11)6/42 (14)82/638 (13)
Rattus nitidus0/1 (0)0/1 (0)
Rattus norvegicus0/2 (0)0/2 (0)
Rattus rattus157/815 (19)137/608 (23)85/282 (30)40/158 (25)419/1,863 (22)
Rattus sabanus0/1 (0)0/1 (0)
Rattus surifer0/14 (0)0/5 (0)0/19 (0)
Tupaia glis1/29 (3)0/20 (0)1/49 (2)
    Total212/1,549 (14)188/1,162 (16)109/496 (22)57/291 (20)566/3,498 (16)
Table 5

Orientia tsutsugamushi infection in Bandicota indica, Rattus losea, and Rattus rattus collected from three villages in northern Thailand during the period 1992–2001

MaeSadPaGookNongkroug
TotalTotalTotal
Infection statusno. (%)Mean no of chiggers (± SEM)*no. (%)Mean no. of chiggers (± SEM)*no. (%)Mean no. of chiggers (± SEM)*
* Mean in the same row followed by the same letter are not significantly different (analysis of variance with Tukey’s Mean Separation Procedure; P < 0.05).
Bandicota indica
    Infected29 (9)46.7 (10.7)a19 (19)43.5 (13.6)a1 (12)15.0 (–)
    Uninfected307 (91)56.2 (4.2)a80 (81)53.8 (13.4)a7 (88)50.1 (19.9)a
    Total336 (100)55.4 (3.9)a99 (100)51.8 (11.1)a8 (100)45.8 (17.8)a
Rattus losea
    Infected29 (7)24.4 (5.4)a40 (25)37.5 (8.5)b11 (22)38.6 (12.9)b
    Uninfected282 (93)19.1 (1.3)a123 (75)31.7 (3.5)b38 (78)55.2 (11.2)c
    Total411 (100)19.4 (1.3)a163 (100)33.1 (3.4)b49 (100)51.4 (9.1)c
Rattus rattus
    Infected16 (14)69.6 (17.7)b427 (27)50.1 (3.2)a34 (18)78.9 (11.4)c
    Uninfected98 (86)36.6 (5.3)a1,160 (73)48.2 (2.0)b150 (82)65.1 (5.8)c
    Total114 (100)41.2 (5.3)a1,587 (100)48.7 (1.7)a184 (100)67.6 (5.2)b
Figure 1.
Figure 1.

Provincial map of Thailand showing the eight provinces in which rodents were collected.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 69, 5; 10.4269/ajtmh.2003.69.519

Authors’ addresses: Russell E. Coleman, Taweesak Monkonna, Panita Tanskul, Inkam Inlao, Nittaya Khlaimanee, and Kriangkrai Lerdthusnee, United States Army Medical Component, Armed Forces Research Institute of Medical Sciences, 315/6 Rajvithi Road, Bangkok, 10400 Thailand. Kenneth J. Linthicum, California Department of Health Services, Ontario, CA 91764. Daniel A. Strickman, Walter Reed Army Institute of Research, Silver Spring, MD 20910. Stephen P. Frances, Australian Army Malaria Institute, Gallipoli Barracks, Enoggera, Brisbane, Queensland 4051, Australia. Thomas M. Kollars, Jr., Entomological Sciences Program, U.S. Army Center for Health Promotion and Preventive Medicine, Aberdeen Proving Ground, MD 21010. Pochaman Watcharapichat, Duangporn Phulsuksombati, and Noppadon Sangjun, Research Division, Royal Thai Army Component, Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand.

Acknowledgments: We thank Siriporn Mungviriya and Warisa Leepitakrat for assisting with data entry.

Financial support: Funding for this project was provided by the Military Infectious Diseases Research Program of the U.S. Army Medical Research and Materiel Command (Fort Detrick, Frederick, MD).

Disclaimer: The opinions of assertions contained in this manuscript are the private ones of the authors and are not to be construed as the official or reflecting views of the Department of Defense or the Armed Forces Research Institute of Medical Sciences.

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Author Notes

Reprint requests: Department of Entomology, Armed Forces Research Institute of Medical Sciences, 315/6 Rajvithi Road, Bangkok 10400, Thailand.
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