Jpn. J. Infect. Dis., 60, 271-279, 2007
Original Article Emergency Vector Control in a DENV-2 Outbreak in 2002 in Pingtung City, Pingtung County, Taiwan Hwa-Jen Teng*, Tzay-Jinn Chen1, Shu-Fen Tsai, Chiung-Pin Lin, Horng-Ying Chiou, Min-Cheng Lin, Shih-Yan Yang, Yi-Wun Lee, Chi-Chieh Kang2, Ho-Cheng Hsu3 and Niann-Tai Chang4 Centers for Disease Control, Department of Health; 1Department of Health, Executive Yuan, Taipei; 2Bureau of Health and 3Bureau of Environmental Protection, Pingtung County Government; and 4National Pingtung University of Science and Technology, Pingtung, Taiwan (Received January 9, 2007. Accepted June 6, 2007) SUMMARY: This paper reports the strategy and effectiveness of an emergency control program conducted in Pingtung City, Taiwan in response to dengue outbreaks. In our control strategy, we carried out 3 insecticide space sprays with an interval of 6-7 days and 2 source reductions to cover the entire duration of dengue virus exposure in humans and mosquito vectors. The control effect was demonstrated by a significant reduction in the Breteau (51.1%) and larval (80.0%) indices, but no such effect was demonstrated by alterations in the adult index (54.9%), house index (45.0%), container index (33.8%), or by indoor (15.8%), outdoor (31.2%), or total water-filled containers (22.7%) per 100 premises examined. The contribution made by the reduction in the number of positive containers was primarily in the outdoor (77.2%), and not the indoor containers (–6.0%). This reduction attributed to an overall reduction of 96.0% Aedes albopictus larvae and 71.0% Aedes aegypti. Therefore, 4 weeks after this extensive emergency control measure, the number of dengue cases dropped to one. Finally, due to both the decrease in temperature resulting from the upcoming winter, and to the sustained effort toward source reduction, the transmission cycle of DENV-2 in Pingtung City was interrupted at the beginning of 2003, and no additional cases were identified in late 2003.
vectors of dengue in Taiwan. The distribution of the former INTRODUCTION species is geographically limited to areas south of the northern Dengue fever is a travel-related disease in Taiwan, as trav- Tropic of Cancer (9,10), and this species is more important elers can carry dengue virus (DENV) from endemic areas than the latter in the epidemiology of dengue in southern into the island. After being transported to the island, this Taiwan, which includes Pingtung City. Ae. albopictus indi- virus is passed on to Aedes mosquitoes, which can cause an viduals are distributed throughout the island. This mosquito outbreak of dengue fever. Several historical outbreaks were is responsible for epidemics of dengue, e.g., small outbreaks documented before World War II, and the last one was recorded in Chungho, Taipei County in 1995 (162 cases), Tung-Hai in 1942-1943 throughout Taiwan. The virus had been silent University in Taichung in 1995 (8 cases), and Taipei City in for 37 years, until a DENV-2 outbreak occurred in 1981 on 1996 (14 cases) that have occurred in areas without Ae. aegypti a remote islet of Hsiao-Liuchiu. Fortunately, the dengue (11,12). Therefore, due to the presence of these two efficient outbreak did not result in an epidemic in Taiwan proper. dengue mosquito vectors and the introduction of DENVs, Later, a DENV-1 epidemic exploded in 1987-1988 in south- Taiwan has experienced small to moderate dengue outbreaks ern Taiwan. In 1987-2002, the epidemic patterns of dengue from time to time. Two major outbreaks with DENV-1 (4,389 in Taiwan cycled with small-scale outbreaks occurring al- cases) and DENV-2 (5,336 cases) occurred in 1988 and 2002, most every 3 years, and large-scale epidemics occurring nearly respectively, because the transmission cycle was not interrupted every 10 years (1). Most local outbreaks began in June-July, during the previous year. To terminate virus transmission peaked in October-November, and ended in December to within 1 year in Taiwan, it is important to prevent dengue January - February of the next year, depending on control endemics from developing into epidemics and to reduce the efforts. However, with the exception of two large outbreaks chance of acquiring dengue hemorrhagic fever (DHF)/dengue in 1988 and 2002, cases originating from these 2 years were shock syndrome (DSS) cases. found year-round. A previously developed dengue vaccine is Studies have suggested that the severity of dengue at the promising, but remains at the clinical trial stage (2-6). There- level of secondary infection depends on the interval between fore, countries with vector mosquitoes should have a control the initial DENV-1 infection and the secondary DENV-2 strategy and emergency infrastructure in place to stop the infection (13), as well as on the type of virus, especially in the transmission cycle during an outbreak. A prevention strategy case of DENV-2 (14,15). The transition from dengue fever to that maintains mosquito density at or below a 1% house DHF and DSS in Taiwan was seriously challenged in 2002 index can effectively reduce the threat of epidemics (7,8). by a DENV-2 outbreak with an interval of 14 years since the Aedes aegypti L. and Aedes albopictus Skuse are the main DENV-1 endemic in 1988. In 2002, there were 20 fatalities among 240 DHF cases (8.75% case fatality) (16). Multiple *Corresponding author: Mailing address: Centers for Disease circulating serotypes were also detected in the small outbreaks Control, Department of Health, 161 Kun-Yang Street, Taipei, of 2003 (types 1 and 2), 2004 (types 1 and 4), and 2005 (types Taiwan 11561. Tel: +886-2-26531385, Fax: +886-2-27822319, 2 and 3). Therefore, it has been essential to build and main- E-mail: [email protected] tain an efficient emergency infrastructure that would enable
271 a rapid response to epidemics in order to protect high-risk year, with the rainy season lasting from May to October. This populations in southern Taiwan. Unfortunately, since the last city experienced in DENV-1 outbreaks in 1987, 1988, and outbreak, no optimal example of emergency preparedness 1995; no outbreaks occurred in the period from 1996-2001. has yet been identified (17). To date, most publications on The case distribution in 79 wards of Pingtung City in an out- dengue outbreak have dealt with epidemiology and vector break occurring in 2002 is presented in Fig. 1B. Both dengue surveillance (7,18-21). vectors, Ae. aegypti and Ae. albopcitus, can coexist in the In order to provide an example of emergency vector control same city; however, Ae. aegypti is found primarily in the center in response to dengue outbreaks, we outline here the strategy of the city, while Ae. albopictus inhabits primarily the city for and effectiveness of an emergency control program con- boundaries (Fig. 1C). ducted in Pingtung City, Pingtung County, Taiwan. The present Control strategy: Financial and human resources reserved control strategy entailed spreading 3 rounds of insecticide for dengue control in response to outbreaks will always be spray and implementing 2 rounds of source reductions to associated with difficult allocation issues. Emergency con- cover the entire durations of potential exposure to DENVs in trol measures should focus on areas in which dengue vectors humans and vectors. The present approach included inhibit- thrive (in our case, first-floor premises and basements). In ing the ability of mosquitoes to lay eggs on less preferable addition to their presence of infectious mosquitoes, viruses are water-holding sites in their struggle for survival, as well as also found in patients during the viremic phase, which lasts prevention of partial failures during the execution of control for 4-5 days (Fig. 2) (22,23). Emergency insecticide spray measures. The methods used for the evaluation of this pro- for killing infected adult mosquitoes, should be applied up to gram are also discussed below, in order to facilitate improve- three times, intervals of 7 days, to cover the intrinsic incuba- ments to such programs to prevent future outbreaks. tion (4-7 days) and infectious (0-5 days) periods affecting patients with dengue (23) who are within the flight range of mosquitoes. In order to interrupt the transmission cycle, it MATERIALS AND METHODS is critically important to reduce the probability of a dengue Description of the control area: The program described patient being bitten by a female vector. In addition to health here, implemented to control the transmission of a dengue education campaign regarding personal protection, two series outbreak in 2002, was conducted in Pingtung City, which is of source reduction should be applied at an interval of 7 days located at 22°43´-22°36´N and 120°26´-120°32´E (Fig. 1A). in order to remove mosquito larvae from the premises of Pingtung City is a medium-sized city (approximately 65.1 infected patients; this measure aims to prevent the spread of km2 in area) with 65,750 households (215,520 inhabitants) disease due to dengue patient mobility. Effective coverage in Pingtung County, Taiwan. The average temperature is 25°C by insecticide spray and source reduction are both critical for and the total annual precipitation is approximately 2,000 mm/ the success of a control program. In our program, we included
Fig. 1. The control city in a Taiwan map (A), the number of dengue confirmed cases in each ward of Pingtung City (B), and the distribution of Aedes aegypti in Pingtung City (C) based on a 2003 survey; black areas indicate that either Ae. aegypti larvae or adults were collected at least once, gray areas indicate that no Ae. aegypti were collected, and white areas indicate that no surveys were conducted.
272 dents were also carried out at that time in the affected areas. Extensive emergency mosquito control measures: The insecticide space sprays were carried out three times, i.e., on November 20-24 (first round), November 26-December 1 (second round), and December 3-6 (third round) in 2002, in intervals of 6-7 days. Ultra low volume (ULV) or aerial space spray was applied to the interior of each house, while fogging/ ULV/aerial space spray was used on outdoor resting sites for mosquitoes at 8:30-11:30 and 14:00-16:40. The portable machines that most commonly used were fogger models K-10 SP (pulsFOG, Überlingen, Germany) and SS-150 (Seshin Industrial Co., Daegu, Korea), ULV Colt (London Fog, Inc., Long Lake, Minn., USA) and Solo 423 and 450 (Solo, Newport News, Va., USA). The active ingredients of the insecticide, Perdelta EC (Aerolead International, Ltd., Taoyuan, Taiwan), were Deltamethrin and Permethrin (0.5 and 7.0% AI, respectively). The total amount of Perdelta used Fig. 2. Conceptual framework of a control strategy in response to the was approximately 860 L (bottles). The application rates were outbreak in Pingtung City, Pingtung County, Taiwan in 2002. (During recommended at 2.5, 0.375, and 2.5 mg/100 m2 for the space an outbreak, viruses are found in infectious mosquitoes and patients in spray, ULV, and fogging, respectively. This chemical was the viremic period shortly before the onset of symptoms and generally lasts 4-5 days) and, later, will be found in infected persons by the tested in bioassays of field-caught females to ascertain the bite of infectious mosquitoes. Infected persons will go through an susceptibility of the vectors. Operators were provided by the intrinsic incubation period (4-7 days) and a viremic period. When a army, the Environmental Protection Agency (EPA) of the female mosquito takes an infected blood meal, a minimum of 8-12 Taipei Municipal Government, and a private pest control busi- days will be needed for virus replication before this mosquito becomes ness. Each team consisted of 1 leader with an EPA profes- infectious with the ability to transmit the virus. sional license as a pest control operator, 3 operators, 2 scouts for health education and source reduction, 1 police officer, 63, 43, and 23 wards in the first, the second, and third insecti- and 1 locksmith to unlock doors when no residents were cide applications, respectively; source reduction was carried at home. Bioassays were provided for each spray team to out twice across the entire city (79 wards). ascertain the quality of the insecticide spray. Except for the Dengue surveillance system, laboratory diagnosis, and first application, all insecticide applications were conducted routine emergency control measures: Dengue is classified under law enforcement. This was the first time police offi- as a notifiable disease in Taiwan, which requires physicians cers were included in the process of insecticide application to report the infection within 24 h of clinical diagnosis. All in Taiwan. serum specimens collected from suspected cases were tested Disease control was defined by the Control of Communi- by capture IgM and IgG enzyme-linked immunosorbent cable Diseases Act, which was re-amended on 1 January 2002. assay (ELISA). If specimens were collected within 7 days of According to the law on the Control of Communicable Dis- disease onset, reverse transcription-polymerase chain reac- eases, Article 28 (36 in the most recent version) (25), a local tion (RT-PCR) and virus isolation were also carried out. A governing agency can enter public or private places to conduct confirmed dengue case was defined as follows: (i) positive disease control measures with the assistance of village leaders for DENV isolation; (ii) positive real-time one-step RT-PCR and other related officers (e.g., the police). In the case of test; (iii) positive seroconversion or ≧ four-fold increase in prevention of a dengue outbreak, disease control measures the amount of dengue-specific IgM or IgG antibody from ap- against dengue vector mosquitoes include insecticide sprays propriately timed paired serum sampling; or (iv) high-titer and source reduction. If an individual refuses, avoids, or dengue-specific IgM and IgG antibody in a single serum speci- jeopardizes the control measures, it may constitute not only men, in which cross-reaction with Japanese encephalitis had immediate mandatory prosecution (including the unlocking been excluded. The detailed protocol for each method is of a door by a locksmith), but may also result in a fine ranging described in a paper by Shu et al. (24). Laboratory results from NT$ 60,000 to NT$ 300,000. In addition to this article, were to be completed within 24 h for ELISA, 48 h for RT- article 23 (25 in the most recent version) reinforces that local PCR, and 14 days for virus isolation. The results were faxed residents conduct source reduction themselves after such to local public health bureaus as soon as possible for further notice and announcement by local governments. If breeding action. Local public health personnel then conducted an epide- containers with Aedes larvae are found in private houses, miological survey of the patients and their contact persons to owners are fined in amounts ranging from NT$ 10,000 to identify the DENV source. In cases of local mosquito trans- NT$ 150,000. mission, an additional 100 blood samples were drawn to find The first floors of houses as well as basements in the entire the possible source of infection and to determine the degree city were inspected twice by 120 temporary workers from of virus spread within the neighboring 50 households. For November 18-22 and 25-29, respectively, to remove all con- each suspected case, the local government carried out a space tainers. These 120 workers had conducted an entomological spray of the interior of all houses and outdoor mosquito rest- survey for months beforehand and formed 40-60 teams with ing sites within a 50-meter radius of that case’s residence and 2-3 persons per team. All containers were eliminated if they workplace. When a case was confirmed by laboratory diag- were not wanted, or were treated as follows: the water was nosis, another follow-up spraying was performed 7 days in replaced in ornamental plant vases, and unused containers order to kill any newly infected mosquitoes. In addition, larval were turned upside-down; water storage containers were also surveys, source reduction, and health education for local resi- either covered, or a larvicide (Vectobac G, 200 International
273 Toxic Units/mg; Abbott Laboratories, North Chicago, Ill., versus outdoor), and were brought back to the laboratory in USA) was applied to large water containers and other breed- iceboxes; and specimens were stored at –20°C until virus de- ing sites. All larvae were identified on the site as belonging tection. The Flavivirus Laboratory of the Centers for Disease the Aedes genus by a visual examination carried out by the Control (CDC)-Taiwan carried out virus detection by a one- inspectors. step SYBR Green I-based real-time RT-PCR Assay, which has Evaluation methods: Multiple methods were used to evalu- been described in Shu et al. (26). The number of mosquitoes ate these emergency mosquito control measures. The num- per pool ranged from 1 to 28. ber of human dengue cases were monitored by onset week, The adult index (the number of Aedes females collected and mosquito surveys were performed before and after the per premise) was used to measure adult density. Traditional indicated measures had been carried out. Mosquito surveys Stegomyia indices, i.e., the house index (the percentage of were carried out 1-2 weeks before (October 29-November houses that are positive for Aedes larvae or pupae), the Breteau 6) and after control measures (on December 3-6) were taken. index (the number of containers that are positive for Aedes Before the extensive emergency control measures were ap- larvae or pupae per 100 houses), the container index (the per- plied, surveys were conducted in all 38 suspected cases and centage of water-filled containers that are positive for Aedes surroundings within a radius of 100 meters; a total of 3,238 larvae or pupae), and the larval index (the number of Aedes premises were inspected in this manner to identify control larvae and pupae per 100 premises), were used. In two wards, problems and notify the local government. At the same time, 150 ovitraps were placed outside of houses and these traps the spray quality was monitored by operators. Nine wards were checked weekly. Each ovitrap was a black polyethylene (867 premises total) were selected from the areas of distribu- cylinder (height, 11cm; diameter, 12 cm) lined with a strip of tion of Ae. aegypti and Ae. albopictus in order to evaluate the paper and filled with water to 2/3 of the total height. control effect using a paired t test. After extensive control measures were performed from December 3 to 6, the same RESULTS survey as that carried out prior to treatment was again con- ducted at a total of 964 premises in these wards. Larvae and Condition before emergency control measures: Before adults were collected by dippers and sweeping nets, respec- the extensive control measures were carried out, the number tively, and species were identified microscopically. Collected of indigenous dengue cases per week from October 27 to adults were pooled by species, sex, and collection site (indoor November 9 was 32 (Fig. 3). For all 3,238 premises surveyed,
Fig. 3. Human dengue cases by onset week in Pingtung City, Pingtung County, Taiwan, 2002 along with the weather data of temperature, relative humidity, and precipitation. Routine control measures by local government included 1 or 2 space sprays and 1 source reduction by larval surveys within a 50-meter radius of the case’s residence and workplace, and health education of local residents. In survey before control, activities included larval and adult surveys within a 100-meter radius of the case’s residence and workplace, the detection of mosquito infection and spray quality monitoring to identify the problem in this ongoing outbreak by professional teams.
274 DENV-2 were detected from 2 pools (1 pool with 2 females outdoor 7.8%), and pottery pots (indoor 0.3%, outdoor 2.9%) and 1 pool with 1 male) of Ae. aegypti, which were collected (Table 2). This information was forwarded to the correspond- inside of the first floors of houses (Table 1). Breeding con- ing teams to carry out source reduction and to educate local tainers with dengue vectors in Pingtung City were mostly residents. found outdoors (61.6%). The key containers, represented as Emergency extensive mosquito control measures: Wards the percentage of total positive containers, were as follows: with Ae. aegypti were subject at least twice to insecticide flower vases (indoor 29.6%, outdoor 11.7%), water buckets spraying, and wards with Ae. albopictus were sprayed only (indoor 2.1%, outdoor 19.2%), plant saucers (indoor 1.8%, once (Fig. 4A). The number of wards subjected to one, two,
Table 1. Dengue virus isolation from mosquitoes collected from Oct. 29 to Nov. 6, 2002 in Pingtung City, Pingtung County, Taiwan before the emergency extensive control to find the possible infection sites of dengue inside or outside the house No. of mosquitoes assayed Dengue viruses Species and No. of pool by RT-PCR detected MIR3) collection site tested1) ♀ ♂ No. Type Aedes aegypti 55 62 85 22) 2 13.61 Indoor 37 41 70 2 2 18.02 Outdoor 18 21 15 0 0.00 Aedes albopictus 12 18 7 0 0.00 Indoor 2 4 0 0 0.00 Outdoor 10 14 7 0 0.00 1): The number of mosquitoes were pooled from 1 to 28. 2): Two positive pools include 1 pool with 2 females and 1 pool with 1 male. 3):MIR, minimum infection rate per 1,000 mosquitoes determined from reverse transcription- polymerase chain reaction (RT-PCR) results.
Table 2. The type of water-filled containers and positive containers inspected in mosquito surveys before the emergence extensive control program (Oct. 29-Nov. 6), in the first and the second source reductions (Nov. 18-22 and Nov. 25-29, respectively) Before emergency extensive First source Second source control program reduction reduction Container type Total positive Total Positive Total Positive Indoor (%) Outdoor (%) containers containers containers containers containers Flower vase 159 29.6 11.7 3,497 212 2,526 73 Water bucket 82 2.1 19.2 2,243 52 1,583 60 Plant saucer 37 1.8 7.8 2,292 43 1,724 13 Pottery pot 12 0.3 2.9 898 25 709 7 Tin can 11 0.5 2.3 339 10 209 6 Cup 7 0.0 1.8 157 3 75 3 Plastic basket 6 0.0 1.6 195 9 115 7 Polyester container 3 0.0 0.8 198 5 92 7 Used tire 4 0.3 0.8 316 6 144 2 Basement 2 0.5 0.0 15 0 35 0 Others 62 3.4 12.7 1,461 55 1,052 24 Total 385 38.4 61.6 11,611 420 8,264 202
Fig. 4. Areas that were covered by insecticide space spray (A) and source reductions (B).
275 Table 3. Spray coverage in three rounds of insecticide space spray of deltamethrin and permethrin (0.5 and 7.0% AI, respectively) in Pingtung City, Pingtung County, Taiwan from Nov. 20 to Dec. 6, 2002 Ward spray No. of premises sprayed No. of Spray time frequency Total2) Partial2) 1) wards Absent Refusal (%) Total in total coverage coverage Nov. 20-24 1 time 33 6,561 451 467 217 ( 2.8) 7,696 (1st round) 2 times 17 4,071 239 511 215 ( 4.7) 5,036 3 times 13 2,054 258 271 359 (12.2) 2,942 Total 63 12,686 948 1,249 791 ( 5.0) 15,674 Nov. 26-Dec. 1 1 time 3 560 307 122 19 ( 1.9) 1,008 (2nd round) 2 times 27 10,434 971 1,708 422 ( 3.1) 13,535 3 times 13 5,060 807 910 182 ( 2.6) 6,959 Total 43 16,054 2,085 2,740 623 ( 2.9) 21,502 Dec. 3-6 2 times 10 3,615 635 476 77 ( 1.6) 4,803 (3rd round) 3 times 13 3,318 1,589 147 24 ( 0.4) 5,078 Total 23 6,933 2,224 623 101 ( 1.0) 9,881 1):Ward spray frequency in total: 1 time indicated the ward received insecticide spray once at that round only, 2 times indicated the wards received insecticides sprays twice (one spray at that round and the other spray in the other round) and 3 times indicated the wards received insecticide spray three times (one spray at each round). 2):Total coverage refers to the spraying of all rooms, and partial coverage indicates that at least one room was not sprayed due to a difficulty. or three insecticide sprayings was 36, 27, or 13, respectively eggs per ovitrap during the control period was 10.7 eggs dur- (Table 3). Law enforcement officials increased the number ing the period from November 24 to 30, and increased to of premises (6,959 and 5,078 in the second and third rounds) 16.0 eggs by the next week. A sharp drop in female oviposi- in 13 wards that completed 3 rounds of insecticide spraying tion activities was detected immediately after the completion (2,942 households were include in the first round). Premises of insecticide spraying (Fig. 5). with no one at home (910 and 147 premises in the second A control effect was also demonstrated by a significant and third rounds, respectively) were unlocked by locksmiths. reduction in the Breteau index (51.1%) (t = 2.59, df = 8, P < Inhabitants who refused (affecting 182 and 24 premises in 0.05) and the larval index (80.0%) (t = 2.94, df = 8, P < 0.05), the second and third rounds) were subject to prosecution but not in the house index (45.0%), container index (33.8%), and a fine. Seventy-eight wards were included in the first and or in the number of indoor (15.8%), outdoor (31.2%), or total second source reductions (Fig. 4B). The number of houses water-filled containers (22.7%) per 100 premises (Table 4). inspected during the first and second rounds of source reduc- The contribution made by the reduction in the number of tions was 21,659 and 22,759 premises, respectively. The num- positive containers was derived primarily from outdoor con- ber of water-filled containers checked was 11,611 and 8,264 in tainers (77.2%) (t = 3.04, df = 8, P < 0.05), not from indoor the first and second source reductions, respectively (Table 2). containers (–6.0%). The average number of positive outdoor Of these containers, 420 (3.6%) and 202 (2.4%) were positive containers per 100 premises was reduced from 6.56 to 1.49, in the first and second source reductions, respectively. while the average number of positive indoor containers per Evaluation of the control effect: Good control was achieved 100 premises remained basically consistent (3.06 and 3.24 at in terms of the number of human dengue cases by onset week, pre- and post-treatment, respectively). The average number and by larvae and oviposition data, with respect to the adult of Ae. albopictus larvae per premise was significantly reduced index. The number of human dengue cases slowly increased (96.0%) (t = 2.44, df = 8, P < 0.05), i.e., from 1.19 to 0.05, starting in July 28, and peaked from October 27 and Novem- and that of Ae. aegypti larvae was also reduced (71.0%) (t = ber 9 (Fig. 3). Starting during the period from November 10 2.35, df = 8, P < 0.05) from 2.14 to 0.62. to 16, experienced entomological control teams were involved in the routine emergency control measures, i.e., supervising DISCUSSION insecticide sprays within a radius of 50 meters and carrying out larval and adult surveys within a radius of 100 meters The success of an emergency control program to stop the in each suspected case. In the period from October 27 to transmission of DENV depends not only on early intervention November 9, the number of cases dropped from 32 to 21. by early detection, but also on a reduction of vector density, When all control measures were interrupted between Novem- as observed in the field, to the transmission threshold defined ber 10 to 16 to prepare for the following campaign, the for each location (27). Based on simulations, the percentage number of dengue cases linearly increased from 21 to 23 and of control needed to stop transmission may vary from 10 to then to 27 during the following 2 weeks. In the period from 96% at different locations. In our example, the reduction December 1 to 7 (1 week after the second application), the of mosquito vectors plus a periodic cleaning effect achieved number of cases dropped by one-half, and then continually by two source-reduction events was found to be an effective dropped to 1 case from December 29, 2002 to January 4, strategy for halting the transmission of DENV infection. In 2003. A 54.9% reduction in the adult index was achieved by this study, 4 weeks after these extensive control measures were the use of insecticide spray and source reduction, but only a carried out, only one remaining dengue case was identified. small number of adults was collected during pretreatment Finally, low temperatures due to the upcoming winter, com- (0.007 females per premise) (Table 4). The mean number of bined with sustained efforts at source reduction, led to termina-
276 Table 4. Density change of immatures and adults reflected in control effects between pretreatments (Oct. 29-Nov. 6) and posttreatments (Dec. 3-6) No. of Pretreatments Posttreatments Categories1) Reduction (%)3) Paired t test wards2) (mean per ward) (mean per ward) Adult index 9 0.007 0.003 54.9 t = 1.78, P = 0.11 House index 9 7.08 3.90 45.0 t = 2.06, P = 0.07 Container index 9 14.33 9.49 33.8 t = 1.92, P = 0.09 Breteau index 9 9.67 4.73 51.1 t = 2.59, P = 0.03 Indoor positive 9 3.06 3.24 –6.0 t = –0.14, P = 0.89 containers Outdoor positive 9 6.56 1.49 77.2 t = 3.04, P = 0.02 containers Larval index 9 332.67 67.30 80.0 t = 2.94, P = 0.02 Aedes aegypti 9 2.14 0.62 71.0 t = 2.44, P = 0.04 larvae per premise Aedes albopictus 9 1.19 0.05 96.0 t = 2.35, P = 0.047 larvae per premise Total containers per 9 70.54 54.49 22.7 t = 1.34, P = 0.22 100 premises Indoor containers 9 38.65 32.55 15.8 t = 0.74, P = 0.48 Outdoor containers 9 31.89 21.94 31.2 t = 1.46, P = 0.18 1): Adult index, the number of Aedes females collected per premise; house index, the percentage of houses that are positive for Aedes larvae or pupae; container index, the percentage of water-filled containers that are positive for Aedes larvae or pupae; Breteau index, the number of containers that are positive for Aedes larvae or pupae per 100 houses; and larval index, the number of Aedes larvae and pupae per 100 premises. 2): The number of premises surveyed in pre- and post-treatment were 867 and 964, respectively. 3): The reductions were calculated as the difference in the numbers in pre- and post-treatment, which was then divided by the number in pre-treatment.
Fig. 5. Egg oviposition activities in Pingtung City from Nov. 24, 2002 to Jan. 11, 2003, as measured by ovitraps. The temperature and precipitation were recorded by Kaohsiung District Agricultural Research and Extension Station, located in Pingtung City.
277 tion of the transmission cycle of DENV-2 in Pingtung City at Therefore, it is critical to conduct a second round of source the beginning of 2003; no additional cases were identified by reduction during a dengue outbreak, and coverage should take late 2003. The temperature in southern Taiwan in 2003, espe- into account the mobility of all dengue patients. In order to cially in January, was not low enough to stop transmission reduce the number of positive indoor containers, the assistance (the mean temperature in Pingtung City was 18.8°C, and ranged of local residents is needed. Therefore, effective community from 11.7 to 27.7°C), but it did reduce the blood-feeding participation in maintaining a hygienic lifestyle with regard behavior of mosquitoes and inhibited virus amplification. to indoor water-filled containers is critical; the community- Moreover, the personal protection effect was enhanced by based dengue prevention programs in Puerto Rico serve as the wearing long sleeves, and by the closing the windows an example (31). and doors in winter. Surveillance of mosquitoes infected with DENVs provides According to our control strategy, 3 rounds of insecticide early warning of the risk of transmission in a particular area spray and 2 rounds of source reduction were implemented to and information regarding the specific predominant circulat- cover the whole duration of DENV exposure in humans and ing serotype in the vector population (32,33). Control pro- vectors to overcome the instinctual ability of mosquitoes to grams can then be prioritized and focused more effectively at lay eggs on less preferable water-holding sites in a struggle specific locations. In our program, two positive Ae. aegypti for survival and to avoid partial failures in the execution cases were detected from samples collected indoors on the of control measures. However, frequency of rounds of appli- first floor of a house. Hence, it was necessary to spray the cation could be reduced based on the effectiveness of the insecticide indoors, on the first floor, in order to kill any two measures applied. Theoretically, if source reduction is infected mosquitoes. It was noteworthy that one positive case carried out before insecticide spraying, and these two mea- associated with a male Ae. aegypti has been detected in the sures are 100% effective, then only one round of insecticide natural surroundings. This finding demonstrated that either a spraying and one round of source reduction are required. The transovarial or a venereal transmission mechanism of infec- effectiveness of our strategy may have been influenced by tion occurred among mosquitoes in Pingtung, at a minimum other factors such as various blood-feeding behavior of infection rate of 11.76 per 1,000 male mosquitoes. This result females, especially Ae. aegypti (28), and insecticide resistance. was similar to findings reported from Singapore. The mini- Therefore, spraying of the insecticide should be launched mum infection rate of male Ae. aegypti and Ae. albopictus rapidly and precisely in order to minimize the impact of feed- were 13.3 and 21.5 per 1,000 male mosquitoes, respectively ing behaviors by reducing the number of infected patients. (34). This finding also suggested that mosquitoes might act Spray coverage, spray quality, and insecticide resistance as reservoirs of DENVs in Pingtung City. Moreover, mos- remain of concerns in developing any dengue emergency quitoes infected by the transovarial route can transmit virus control program due to the potential failure to kill dengue orally in a laboratory setting (35). This implies that dengue vectors (18,29). Spray coverage during the first round (2,942 could become an endemic disease in southern Taiwan at some houses in 13 wards) was largely improved by the use of law point the future. enforcement during the second and third rounds (6,959 and Breaking the transmission cycle of DENVs is not easy, but 5,078 houses, respectively). The refusal rate was thereby it is possible. However, without a sustained and compre- largely reduced from 12.2 to 2.6% and 0.4%. In order to hensive prevention program in place to ensure a long-term detect any loss of insecticide efficacy during an outbreak, it mosquito control, vector mosquitoes will return in the fol- is important that efficacy is monitored and diagnostic dosages lowing year (36), and DENV will eventually emerge in new are used. In addition, a comprehensive pesticide-use policy territories. based on a thorough understanding of insecticide resistance is required country-wide. ACKNOWLEDGMENTS In our program, good control of the number of human This work would not have been possible without the collaboration of dengue cases was observed by onset week, and by the larvae many people from different units, including the Army, Environmental Pro- and oviposition data, but not based on the adult index. The tection Agency of the Taipei Municipal Government, Pingtung County Gov- benefits of using a sweeping net as the adult collection method ernment, Tajen Institute of Technology, Taipei Pest Control Association, and are highly dependent upon personal skill, and this approach CDC-Taiwan. Special thanks are extended to the Flavivirus Laboratory, was not found to be sufficiently sensitive to detect a low den- Research and Development Center, CDC, Taiwan for virus detection in mosquitoes and Shu-Ying Li for valuable comments on the manuscript. sity of mosquitoes. It is also possible that larval competition was reduced by vector control measures as well as by the reduced availability of water-filled containers, especially REFERENCES indoor containers. A combination of the Breteau and larval 1. King, C.C., Wu, Y.C., Chao, D.Y., et al. 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