Abstract
Vivax malaria is a significant military and civilian health threat in the north of the Republic of Korea (ROK). The island of Baengnyeong-do is the westernmost point of the ROK and is located close to the southwestern coast of the Democratic People's Republic of Korea (DPRK). Mosquitoes were collected using a black light trap on Baengnyeong-do, and Anopheles spp. were assayed by PCR, to identify the species, and screened for sporozoites of Plasmodium vivax. Of a subsample of 257 mosquitoes, Anopheles lesteri was the most frequently collected (49.8%), followed by Anopheles sinensis (22.6%), Anopheles pullus (18.7%), Anopheles kleini (7.8%), and Anopheles belenrae (1.2%). The overall sporozoite rate was 3.1%, with the highest rates observed in An. kleini (15.0%), An. sinensis (5.2%), and An. lesteri (1.6%). No sporozoite positive An. pullus or An. belenrae were observed. The results extend our knowledge of the distribution and potential role in malaria transmission of An. kleini, An. lesteri, and An. sinensis, for an area previously considered to be at a low risk for contracting vivax malaria.
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Key words: Anopheles lesteri, Anopheles kleini, Anopheles sinensis, Plasmodium vivax, malaria, sporozoite, Baengnyeong-do (Island)
Prior to being eradicated from the Republic of Korea (ROK) in 1979,
Plasmodium vivax Grassi and Feletti, the causative agent of vivax malaria, was endemic and widespread throughout the ROK [
1,
2]. In 1993, vivax malaria reemerged on the Korean peninsula [
2,
3], and in the ROK, most malaria cases have since been contracted near the demilitarized zone (DMZ) that borders North Korea (Democratic People's Republic of Korea, DPRK) [
4-
6]. Unique conditions in the vicinity of the DMZ, such as the exposure of large numbers of soldiers to malaria parasites and the unmanaged nature of the environment that encourages mosquito breeding, are thought to exacerbate the malaria situation [
2,
7]. Little information is available as to how widespread malaria is in the DPRK, what mosquito species are involved in malaria transmission, and the relative abundance and distribution of potential malaria vector populations. Ongoing mosquito surveillance data is available for the ROK [
5,
6] and parasite rates for different species have been reported [
8,
9], but few data of a similar nature are available for the DPRK.
Anopheles belenrae Rueda,
Anopheles pullus Yamada, and
Anopheles sinensis Wiedemann have been recorded in the DPRK in 2 provinces (Hwanghae and Pyongyang) by Rueda and Gao [
10]. Foley et al. [
11] produced ecological niche models for 8 anopheline species using collection location data from the ROK that predicted suitable habitat in the ROK and southern DPRK.
An. sinensis is the predominant species collected south of Seoul; however, in malaria risk areas in the north, other species are frequently more common [
4,
12] and may play a greater role in malaria transmission.
Baengnyeong-do is a 45.8 km
2 island located near the Northern Limit Line (
Fig. 1). This island is the westernmost point of the ROK, and is 16 km from the DPRK coast. As such, entomological conditions on Baengnyeong-do may more closely reflect those in the southwestern DPRK than the rest of the ROK. We collected mosquitoes from Baengnyeong-do in 2007 to better understand the composition of mosquito species and their potential role in malaria transmission in locations where ROK military are deployed.
Mosquitoes were collected using a black light trap near a cowshed on 15 July 2007 at Baengnyeong-do, Jinchon-2ri, Baengnyeong-myeon, Ongjin-Gun, Incheon, 37° 57' 24.5'' N 124° 41' 55.5'' E. Specimens were transported to the 5th Medical Detachment, Yongsan Army Garrison, Seoul, ROK, where they were identified to species or Subgroup using a dissecting microscope and standard keys [
13,
14]. It was impossible to identify members of the
An. sinensis Subgroup (
An. belenrae,
Anopheles kleini,
Anopheles lesteri Baisas and Hu,
An. pullus, and
An. sinensis sensu stricto) by morphological techniques. For members of the
An. sinensis Subgroup, the abdomen was separated from the thorax and head of the mosquito to reduce the probability of detecting DNA from parasite oocysts in the midgut. The head and thorax of a subsample of 257 mosquitoes were identified by PCR for species [
15,
16], and by single step and semi-nested multiplex-PCR to identify
P. vivax sporozoite infections [
17].
A total of 9,971 female mosquitoes were collected (
Table 1), 79.0% of which were
Aedes vexans nipponii Theobald, and 8.8%
Culex tritaeniorhynchus Giles, the primary vector of Japanese encephalitis virus (JEV) in the ROK. Overall,
An. sinensis Subgroup species made up 11.8% of the collections, of which
An. lesteri predominated (49.8%), followed by
An. sinensis (22.6%),
An. pullus (18.7%),
An. kleini (7.8%), and
An. belenrae (1.2%). Overall, the sporozoite rate for members of the
An. sinensis Subgroup was 3.1%, with highest rates in
An. kleini (15.0%), followed by
An. sinensis (5.2%), and
An. lesteri (1.6%). Sporozoite positive
An. pullus and
An. belenrae were not observed (
Table 2).
Ae. vexans nipponii, is considered a nuisance mosquito that is not readily attracted to humans. It is an early-season floodwater mosquito whose populations rapidly increase with the flooding of rice paddies or heavy rains [
5].
Ae. vexans nipponii is usually collected less frequently than members of the
An. sinensis Subgroup in New Jersey light trap catches throughout most of the ROK [
4,
12,
18], but was the most commonly collected species trapped at Baengnyeong-do.
An. lesteri was the most frequently collected anopheline, but is infrequently collected in north Gyeonggi and southern provinces throughout the ROK [
9,
19]. This species is considered an important malaria vector in China [
20], and was found to be infected with
P. vivax, albeit at relatively low rates, in the present study. The highest sporozoite rate was observed in
An. kleini, and we have found this species infected also in northern Gyeonggi province of the ROK (unpublished data). Laboratory experiments found that
An. lesteri and
An. kleini produced many sporozoites, whereas
An. sinensis and
An. pullus produced few sporozoites [
21]. However, in another study, An. pullus was observed by ELISA to have sporozoite infections of >1,000 sporozoites (unpublished data). Although no sporozoite positive
An. belenrae were found in this study, this species has been reported as positive in other studies [
9,
18]. Taking into consideration of the extrinsic incubation period of
P. vivax, the fact that
An. sinensis,
An. lesteri, and
An. kleini were positive for sporozoites, and the remoteness of the island, these species were biting infected humans on Baengnyeong-do, probably 10 days or more beforehand.
As only one trap catch is reported, these results cannot be assumed to reflect conditions for other times of the year, especially during the latter part of summer when normally higher malaria infection rates are observed. For example, relative species abundance and demographic factors, such as longevity, which may predispose mosquitoes for the growth of sporozoites, varies throughout the mosquito season in the ROK [
8] (unpublished data). Also, the presence of sporozoites, while necessary for infection of humans, may not translate to new cases, if the number of sporozoites is low [
22]. Data provided by the Korea Centers for Disease Control and Prevention for years 2001-2010 showed that Incheon Metropolitan city, which includes the remote island Banengyneong-do, had the second highest overall mean number of malaria cases reported [
23], but with low numbers of malaria cases (7 cases) for 2001-2010 reported in Baengnyeong-do [
23]. Baengnyeong-do and possibly nearby areas of the DPRK may be suitable for malaria transmission, although it differs from most of the rest of the ROK in the high frequency of
An. lesteri, limited human population movements, and island environmental conditions.
The Incheon Metropolitan city government has plans to increase access and facilities on the island to attract tourists year-round [
24]. The likelihood of local malaria transmission suggests that active malaria surveillance to reduce asymptomatic cases, vigilance regarding anti-malarial prophylaxis, and vector control is needed, to minimize the potential for the spread of malaria to visitors and residents of Baengnyeong-do.
ACKNOWLEDGEMENTS
Funding for portions of this work was provided by the Armed Forces Health Surveillance Center, Division of Global Emerging Infections Surveillance and Response System, Silver Spring, MD, USA and the National Center for Medical Intelligence, Fort Detrick, MD, USA. This research was performed under a Memorandum of Understanding between the Walter Reed Army Institute of Research and the Smithsonian Institution, with institutional support provided by both organizations. The opinions and assertions contained herein are those of the authors and are not to be construed as official or reflecting the views of the Department of the Army or the Department of Defense.
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Fig. 1Mosquito collection site (○) at a cowshed on Baengnyeong-do in the northwest part of the Republic of Korea.
Table 1.Total numbers of mosquitoes collected by black-light trap near a cowshed in Baengnyeong-do (Island), Incheon, Republic of Korea, on 15 July 2007
Table 1.
|
Species |
Female (%) |
Male |
Total |
|
Ochlerotatus dorsalis (Meigen) |
27 (0.3) |
0 |
27 |
|
Aedes vexans nipponii Theobald |
7,877 (79.0) |
88 |
7,965 |
|
Anopheles sinensis Subgroup |
1,174 (11.8) |
42 |
1,216 |
|
Culex bitaeniorhynchus Giles |
2 (< 0.1) |
0 |
2 |
|
Culex pipiens Linnaeus |
16 (0.2) |
6 |
22 |
|
Culex tritaeniorhynchus Giles |
873 (8.8) |
2 |
875 |
|
Mansonia uniformis (Theobald) |
2 (< 0.1) |
0 |
2 |
|
Total |
9,971 (100.0) |
138 |
10,109 |
Table 2.Total numbers of malaria infected mosquitoes collected and identified by black-light trap near a cowshed in Baengnyeong-do (Island), Incheon, Republic of Korea, on 15 July 2007
Table 2.
|
Species |
Number identified (%) |
Sporozoite rate (%)a
|
|
Anopheles belenrae
|
3 (1.2) |
0.0 |
|
Anopheles kleini
|
20 (7.8) |
15.0 |
|
Anopheles lesteri
|
128 (49.7) |
1.6 |
|
Anopheles pullus
|
48 (18.7) |
0.0 |
|
Anopheles sinensis
|
58 (22.6) |
5.2 |
|
Total |
257 (100.0) |
3.1 |
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