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.
Summary of small mammals collected between 1992 and 2001 in Thailand
| Total number of animals collected | |||||
|---|---|---|---|---|---|
| Adults | Sub-Adults | ||||
| Female | Male | Female | Male | Total | |
| Order Scandentia, Family Tupaiidae (treeshrews) | |||||
| Tupaia glis | 29 | 20 | – | – | 49 |
| Order Insectivora, Family Soricidae (shrews) | |||||
| Crocidura dracula | 1 | – | – | – | 1 |
| Crocidura horsfieldi | 10 | 3 | – | – | 13 |
| Order Rodentia, Family Sciuridae (squirrels) | |||||
| Menetes berdmorei | 17 | 7 | – | – | 24 |
| Order Rodentia, Family Muridae (rats and mice) | |||||
| Bandicota indica | 226 | 130 | 128 | 80 | 564 |
| Bandicota savilei | 17 | 7 | 3 | 3 | 30 |
| Mus caroli | 44 | 18 | 6 | 1 | 69 |
| Mus cervicolor | 11 | 3 | – | 3 | 17 |
| Rattus argentiventer | 9 | 8 | 3 | 3 | 23 |
| Rattus berdmorei | 6 | 3 | – | – | 9 |
| Rattus bowersi | 6 | 3 | – | – | 9 |
| Rattus bukit | 2 | 2 | – | – | 4 |
| Rattus exulans | 84 | 53 | 8 | 1 | 146 |
| Rattus koratensis | 5 | 6 | 1 | – | 12 |
| Rattus losea | 248 | 284 | 64 | 42 | 638 |
| Rattus nitidus | 1 | – | – | – | 1 |
| Rattus norvegicus | 2 | – | – | – | 2 |
| Rattus rattus | 815 | 608 | 282 | 158 | 1,863 |
| Rattus sabanus | – | 1 | – | – | 1 |
| Rattus surifer | 14 | 5 | – | – | 19 |
| Order Carnivora, Family Mustelidae (weasels and otters) | |||||
| Melogale personata | 1 | – | – | – | 1 |
| Order Carnivora, Family Viverridae (civets and Mongooses) | |||||
| Herpestes javanicus | 1 | 1 | 1 | – | 3 |
| Total | 1,549 | 1,162 | 496 | 291 | 3,498 |
Chiggers removed from 16 species of small mammals collected between 1992 and 2001 in Thailand
| Host species | No. of animals infested | No. of animals examined | % infested | Total no. of chiggers collected | Mean no. of chiggers per animal (SEM) |
|---|---|---|---|---|---|
| Bandicota indica | 400 | 557 | 71.8 | 31,581 | 56.7 (4.3) |
| Bandicota savilei | 25 | 30 | 83.3 | 1,332 | 44.4 (6.7) |
| Crocidura horsfieldi | 3 | 13 | 23.1 | 35 | 2.7 (1.5) |
| Menetes berdmorei | 9 | 12 | 75.0 | 636 | 53.0 (19.4) |
| Mus caroli | 33 | 52 | 63.5 | 939 | 18.1 (3.5) |
| Mus cervicolor | 6 | 17 | 35.3 | 226 | 13.3 (6.8) |
| Rattus argentiventer | 21 | 23 | 91.3 | 1,795 | 78.0 (16.5) |
| Rattus berdmorei | 2 | 3 | 66.7 | 70 | 23.3 (14.5) |
| Rattus bowersi | 1 | 1 | 100.0 | 27 | 27.0 (–) |
| Rattus bukit | 3 | 4 | 75.0 | 14 | 3.5 (2.3) |
| Rattus exulans | 33 | 61 | 54.1 | 582 | 9.5 (2.3) |
| Rattus koratensis | 12 | 12 | 100.0 | 1,709 | 142.4 (28.7) |
| Rattus losea | 522 | 638 | 81.8 | 16,309 | 25.6 (1.4) |
| Rattus rattus | 1,499 | 1,781 | 84.2 | 95,896 | 53.8 (1.7) |
| Rattus surifer | 7 | 7 | 100.0 | 406 | 58.0 (20.6) |
| Tupaia glis | 11 | 21 | 52.4 | 2,342 | 111.5 (41.5) |
| Total | 2,587 | 3,240 | 79.8 | 153,899 | 47.5 (1.3) |
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 species | Leptotrombidium chiangraiensis | Leptotrombidium imphalum | Blankaartia sps. | Ascoschoengastia sps. | Not identified | Total collected |
| Bandicota indica | 111 (<1) | 14,802 (47) | 881 (3) | 8,592 (27) | 7,404 (23) | 31,790 |
| Bandicota savilei | – | 352 (26) | 10 (<1) | 583 (44) | 387 (29) | 1,332 |
| Crocidura horsfieldi | – | 20 (57) | – | – | 15 (43) | 35 |
| Menetes berdmorei | – | 293 (46) | – | 159 (25) | 184 (29) | 636 |
| Mus caroli | 30 (3) | 150 (16) | 120 (13) | 633 (67) | 6 (<1) | 939 |
| Mus cervicolor | – | 1 (<1) | – | 225 (9) | – | 226 |
| Rattus argentiventer | – | 888 (49) | – | 75 (4) | 832 (46) | 1,795 |
| Rattus berdmorei | – | 20 (29) | – | – | 50 (71) | 70 |
| Rattus bowersi | – | – | – | 27 (100) | – | 27 |
| Rattus bukit | – | 1 (7) | – | 3 (21) | 10 (71) | 14 |
| Rattus exulans | – | 67 (12) | – | 454 (78) | 61 (10) | 582 |
| Rattus koratensis | – | 1,423 (83) | – | 31 (2) | 255 (15) | 1,709 |
| Rattus losea | 1,537 (9) | 4,351 (27) | 46 (<1) | 6,712 (41) | 3,691 (23) | 16,337 |
| Rattus rattus | 5,023 (5) | 37,905 (40) | 158 (<1) | 13,855 (14) | 38,718 (40) | 95,659 |
| Rattus surifer | – | 100 (25) | – | 96 (24) | 210 (52) | 406 |
| Tupaia glis | – | 2,272 (97) | – | 40 (2) | 30 (1) | 2,342 |
| Total | 6,701 (4) | 62,645 (41) | 1,215 (<1) | 31,485 (20) | 51,853 (34) | 153,899 |
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) | |||||
|---|---|---|---|---|---|
| Adults | Sub-adults | ||||
| Female | Male | Female | Male | Total | |
| Bandicota indica | 17/226 (8) | 10/130 (8) | 15/128 (12) | 10/80 (13) | 52/564 (9) |
| Bandicota savilei | 0/17 (0) | 0/7 (0) | 1/3 (33) | 0/3 (0) | 1/30 (3) |
| Crocidura dracula | 0/1 (0) | – | – | – | 0/1 (0) |
| Crocidura horsfieldi | 0/10 (0) | 0/3 (0) | – | – | 0/13 (0) |
| Herpestes javanicus | 0/1 (0) | 0/1 (0) | 0/1 (0) | – | 0/3 (0) |
| Melogale personata | 0/1 (0) | – | – | – | 0/1 (0) |
| Menetes berdmorei | 0/17 (0) | 0/7 (0) | – | – | 0/24 (0) |
| Mus caroli | 0/44 (0) | 0/18 (0) | 0/6 (0) | 0/1 (0) | 0/69 (0) |
| Mus cervicolor | 0/11 (0) | 0/3 (0) | – | 0/3 (0) | 0/17 (0) |
| Rattus argentiventer | 2/9 (22) | 1/8 (13) | 1/3 (33) | 1/3 (33) | 5/23 (22) |
| Rattus berdmorei | 2/6 (33) | 0/3 (0) | – | – | 2/9 (22) |
| Rattus bowersi | 0/6 (0) | 0/3 (0) | – | – | 0/9 (0) |
| Rattus bukit | ½ (50) | 0/2 (0) | – | – | ¼ (25) |
| Rattus exulans | 0/84 (0) | 2/53 (4) | 0/8 (0) | 0/1 (0) | 2/146 (1) |
| Rattus koratensis | 0/5 (0) | 1/6 (17) | 0/1 (0) | – | 1/12 (8) |
| Rattus losea | 32/248 (13) | 37/284 (13) | 7/64 (11) | 6/42 (14) | 82/638 (13) |
| Rattus nitidus | 0/1 (0) | – | – | – | 0/1 (0) |
| Rattus norvegicus | 0/2 (0) | – | – | – | 0/2 (0) |
| Rattus rattus | 157/815 (19) | 137/608 (23) | 85/282 (30) | 40/158 (25) | 419/1,863 (22) |
| Rattus sabanus | – | 0/1 (0) | – | – | 0/1 (0) |
| Rattus surifer | 0/14 (0) | 0/5 (0) | – | – | 0/19 (0) |
| Tupaia glis | 1/29 (3) | 0/20 (0) | – | – | 1/49 (2) |
| Total | 212/1,549 (14) | 188/1,162 (16) | 109/496 (22) | 57/291 (20) | 566/3,498 (16) |
Orientia tsutsugamushi infection in Bandicota indica, Rattus losea, and Rattus rattus collected from three villages in northern Thailand during the period 1992–2001
| MaeSad | PaGook | Nongkroug | ||||
|---|---|---|---|---|---|---|
| Total | Total | Total | ||||
| Infection status | no. (%) | 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 | ||||||
| Infected | 29 (9) | 46.7 (10.7)a | 19 (19) | 43.5 (13.6)a | 1 (12) | 15.0 (–) |
| Uninfected | 307 (91) | 56.2 (4.2)a | 80 (81) | 53.8 (13.4)a | 7 (88) | 50.1 (19.9)a |
| Total | 336 (100) | 55.4 (3.9)a | 99 (100) | 51.8 (11.1)a | 8 (100) | 45.8 (17.8)a |
| Rattus losea | ||||||
| Infected | 29 (7) | 24.4 (5.4)a | 40 (25) | 37.5 (8.5)b | 11 (22) | 38.6 (12.9)b |
| Uninfected | 282 (93) | 19.1 (1.3)a | 123 (75) | 31.7 (3.5)b | 38 (78) | 55.2 (11.2)c |
| Total | 411 (100) | 19.4 (1.3)a | 163 (100) | 33.1 (3.4)b | 49 (100) | 51.4 (9.1)c |
| Rattus rattus | ||||||
| Infected | 16 (14) | 69.6 (17.7)b | 427 (27) | 50.1 (3.2)a | 34 (18) | 78.9 (11.4)c |
| Uninfected | 98 (86) | 36.6 (5.3)a | 1,160 (73) | 48.2 (2.0)b | 150 (82) | 65.1 (5.8)c |
| Total | 114 (100) | 41.2 (5.3)a | 1,587 (100) | 48.7 (1.7)a | 184 (100) | 67.6 (5.2)b |
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
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
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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