Background: International Health Regulations controls international travel including human movement, disease vector, and imported items to prevent the spread of dengue, especially in seaports, airports, and border crossing posts. This study aimed to determine dengue Transovarial Transmission Index (TTI) and distribution of dengue virus in the areas around Adisucipto Airport of Yogyakarta, Indonesia. Methods: The study was a descriptive analytic study with cross sectional design, conducted by mapping the spread of the dengue virus and identifying TTI in Adisucipto Airport. A total of 145 ovitraps were installed in both perimeter and buffer areas of the airport. Positive Ovitrap Index (OI), TTI, and serotype of dengue virus were examined. The TTI was identified using immunocytochemistry immunoperoxidase streptavidin biotin complex (IISBC) method in mosquito head squash preparations. Results: OI in the buffer area was 32 (45.1%), whereas OI in the perimeter area was 24 (32.4%). The TTI in the buffer and perimeter areas were 21 (18.3%) and 11 (18.9%), respectively. The TTI was found greater in the Aedes aegypti population compared to the Aedes albopictus population, both in the perimeter area (20% versus 16.7%) and the buffer area (20.3% versus 16.1%). Dengue virus serotype-2 (DENV-2) and dengue virus serotype-3 (DENV-3) were predominantly found in Ae. aegypti and Ae. albopictus. Conclusions: Buffer areas of Adisucipto Airport of Yogyakarta have higher risk as breeding sites for Aedes spp., predominantly DENV-2 and DENV-3 serotypes. High OI shows that the areas are likely to have higher risk of developing dengue outbreak. Keywords: Transovarial Transmission Index, Airport, Dengue, Aedes spp. Background on security problems of health and has the potential for In the last 50 years, the dengue disease has been spreading causing an epidemic that can spread across borders rapidly and extensively in the world following the geo- between countries . graphical distribution to many countries, with the tendency Tourists have a major role in the spread of dengue when of spreading from urban to rural areas. An estimated 50 entering areas inhabited with Aedes spp. mosquitoes , million cases of dengue are found every year, and about 2.5 posing a risk of traveler viremia that could carry various billion people are living in dengue endemic countries . strains of dengue serotypes. Study results showed an in- The World Health Organization (WHO) in 2005 issued a creasing trend of dengue cases per year (seasonal) with 522 revision of the rules of international travel, known as the travelers reported by The GeoSentinel Surveillance Net- International Health Regulations (IHR) that included den- work during the peak of dengue cases in Southeast Asia gue as one of the diseases of Public Health Emergency of (June to September), Central Asia (October), South Amer- International Concern (PHEIC) that may have an impact ica (March), and The Caribbean (August, October), all of which indicate the relationship between travel and the oc- currenceof dengueepidemics . In Southeast Asia, the * Correspondence: email@example.com annual morbidity rate has risen from 50 cases per 1000 Center For Tropical Medicine, Faculty of Medicine, Universitas Gadjah Mada, travelers with dengue after traveling to a non-epidemic area Jl. Farmako Sekip Utara, Yogyakarta, Indonesia Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Satoto et al. Environmental Health and Preventive Medicine (2018) 23:22 Page 2 of 7 to 159 cases per 1000 travelers during epidemics , al- This study was conducted to acquire information re- though dengue transmission in the airport has not yet been garding the presence of Aedes spp. mosquitoes and the reported until now. extent of transovarial transmission in the perimeter and The New Tokyo Narita International Airport Quaran- buffer areas of Yogyakarta’s Adisucipto Airport. The tine Post in Chiba Prefecture in year 2000 to 2002 had ex- study was also intended to determine dengue Transovar- amined 233 passengers suspected of being infected with ial Transmission Index (TTI) and distribution of dengue dengue virus: 1 case (4%) out of 26 cases identified in year virus in areas in and around Adisucipto Airport, 2000, 8 cases (12%) out of 69 cases identified in year 2001, Yogyakarta, Indonesia. and 22 cases (16%) out of 138 cases identified in year 2002 were confirmed as dengue infection . Most of the pas- sengers were infected after traveling from Southeast Asian Methods and South Asian countries, one from African countries, This research is a descriptive analytic study with a cross one from Central American countries, one from Central sectional design. The study was conducted by mapping and South American countries, and one from South the spread of dengue virus and identifying TTI in Adisu- American countries . Fever screening in Taiwan Airport cipto Airport of Yogyakarta, Indonesia (07 47′ 17″ Sand begun in July 2003 to June 2004 identified 40 dengue 110 25′ 54″ E). The study was done in December 2015 to cases, among which 33 people (82.5%) were confirmed as May 2016, during which rainy season took place. viremic patients . During 2007 to 2010, sentinel surveil- Dengue cases were collected based on data retrieved lance in Taiwan Airport showed that most of the from local primary health center. All of dengue cases were dengue-infected travelers had just returned from endemic diagnosed with dengue non-structural protein 1 (NS-1) areas around the Southeast Asian region, namely antigen test. However, serotypes of infecting dengue virus Indonesia (21.0 to 35.1%), Vietnam (20.1 to 32.0%), were unknown. The study was conducted by installing Thailand (5.0 to 13.0%), the Philippines (9.0 to 12.3%), 145 ovitraps in both the perimeter and buffer areas of the Cambodia (4.1 to 8.0%), Malaysia (2.0 to 4.1%), Singapore airport. We defined the zones as the following definitions: (1.1 to 3.4%), India (0 to 1.1%), and only few travelers who perimeter area is 100-m peripheral area from airport had just returned from South America (0 to 0.7%) . In apron; buffer area is 400-m peripheral area from airport September 2013, in Germany, a traveler who had just apron . The study could only be performed at the returned from Japan was confirmed as having type 2 den- northern and western area of the airport due to limited gue virus infection; hence, the German Health Authority public access to the eastern and southern area. performed strict monitoring towards travel history of the Ovitrap Index (OI) is calculated from number of ovi- travelers in order to evaluate risk potential of travelers traps with positive eggs divided by sum of ovitraps in- having dengue virus infection . stalled. Ovitraps were installed outdoors and indoors International travel such as human movement, disease within 35–50 m distance. Positive OI and TTI of dengue vector, and contaminated items that potentially cause virus were examined later on. After colonization of Aedes widespread disease are regulated by the WHO in the Inter- spp. eggs, TTI was identified using immunocytochemistry national Health Regulations 2005 Article 9 (nine). Each immunoperoxidase streptavidin biotin complex (IISBC) country is required to perform dengue risk assessment to method in mosquito head squash preparations . Rate prevent the spread of dengue between countries by of TTI was obtained by dividing the number of strengthening surveillance and supervision at the entrance DENV-positive IISBC samples by total number of IISBC areas, i.e., seaports, airports, and border crossing posts . samples examined and was expressed as percentage . According to the Law Act 1 Year 1962 regarding The virus was identified through serotype examination Marine Quarantine and Act 2 Year 1962 regarding Sky by Lanciotti’s RT-PCR. Transovarial transmission in Quarantine, as well as the IHR Year 2005 Article 2, all both Aedes aegypti and Aedes albopictus mosquitoes of which state that seaports and airports are obliged to obtained from indoor and outdoor ovitraps were com- be free from disease vectors and are required to per- pared. The analysis of OI distribution was conducted form disease control and prevention suitable to the po- using the software ArcGIS 9.2 (Esri, New York) to tential risk factors without interfering with the provide mapping and spatial reasoning to yield commercial traffic . Perimeter ports including sea- location-based data. The data were entered into near- ports, airports, and rural ports are expected to be free est neighbor analysis, resulting in the distance between from both larval stage and adult stage of Aedes aegypti each feature centroid and its nearest neighbor’scen- mosquitoes, whereas in the buffer areas the following troid location. The z-score and p value are measures of values are considered essential: House Index (HI) of statistical significance that are used in determining less than, or equal to 1%, Breteau Index (BI) of < 50, whether or not to reject the null hypothesis: features biting rate of < 2.5, and OI of < 15% . arerandomlydistributed. Satoto et al. Environmental Health and Preventive Medicine (2018) 23:22 Page 3 of 7 The presence of high TTI value is considered an im- from outdoor-installed ovitraps, with 16.7% in the per- portant mechanism for the maintenance of the virus in imeter area and 16.1% in the buffer area. Unfortunately, nature and may be associated in the occurrence of den- we did not perform further analysis to identify statistical gue epidemics and outbreak. High OI supports the po- significance of this difference in findings between tential of dengue outbreaks as well . mosquito species. Distribution of dengue virus in the Adisucipto Airport of Yogyakarta was predominantly Results found in zone 4 of the buffer area, the RT 8 of village of Positive OI of Aedes spp. mosquitoes in the buffer area was Maguwoharjo (4 cases or 12.5%), and was least found in 32 (45.1%), with outdoor ovitraps showing greater propor- zone 2, the parking lot and common facility, and zone 3, tion (50%) compared to indoor ovitraps (37.9%). OI in the RT 7 of village of Maguwoharjo, with both areas having buffer area was 32 (45.1%), whereas OI in the perimeter only 1 case detected (3.1%). Dengue virus distribution area was 24 (32.4%) as shown in Table 1.The distribution tends to follow the distribution pattern of ovitraps. In of Aedes spp. mosquitoes based on positive OI in Yogya- both perimeter and buffer areas of the Adisucipto Air- karta’s Adisucipto Airport was found evenly distributed in port, there were no dengue cases found. As described in the surrounding areas, with the highest number of positive Fig. 1, the shortest distance of dengue patients was OI found in the zone 4, the neighborhood 8 (Rukun 389 m, whereas the farthest distance was 1050 m. Tetangga/RT 8) of village of Maguwoharjo (14 ovitraps or The analysis of dengue virus distribution was con- 9.6%), and the least number of positive OI found in zone 4 ducted using the nearest neighbor analysis and resulted of perimeter area, the B Terminal (2 ovitraps or 1.4%) as in z-score of − 2.0 and p value of 0.04 that indicates the shown in Fig. 1. tendency of clustered distribution. The shortest distance The nearest neighbor analysis shows that if the z-score of positive ovitraps was 3.1 m, while the farthest distance is less than 1, the pattern exhibits clustering, whereas if was 33 m with an average distance of 15.2 m. the index is greater than 1, the trend is towards disper- Dengue virus serotype examination was performed in sion. The analysis of OI distribution resulted in z-score dengue-positive Aedes spp. mosquito-colonized samples of − 6.1 and p value of < 0.001 that indicates the ten- and in positive transovarial transmission samples, all of dency of clustered OI distribution. The shortest distance which were coded in species and location. The serotype of positive ovitraps was 3.6 m, while the farthest distance examination was conducted using Lanciotti’s RT-PCR was 19 m with average distance of 13.2 m. The results method and resulted in the detection of DENV-2 and indicate that the distance is still within the range of DENV-3 serotypes in Aedes aegypti and Aedes albopictus mosquito disease transmission. mosquitoes in Adisucipto Airport of Yogyakarta (Table 3). Through identification by examination using immuno- Data analysis on dengue virus serotype distribution in histochemistry (IHC) method, as many as 11 samples Yogyakarta’s Adisucipto Airport resulted in z-score of 1.4 (18.9%) in the perimeter area and 21 samples (18.3%) in and p value of 0.14 that indicates tendency of random the buffer area of Yogyakarta’s Adisucipto Airport were dengue virus serotype distribution. The shortest distance found positive for transovarial transmission. The transo- of dengue virus serotype was 33 m, while the farthest dis- varial transmission was observed higher in percentage in tance was 173 m with average distance of 94.1 m as shown Aedes aegypti mosquitoes, with 20 to 16.7% in the per- in Fig. 2. imeter area and 20.3 to 16.1% in the buffer area (Table 2). In Aedes aegypti mosquitoes, positive transovarial trans- Discussion missions were more commonly detected in samples ob- Ovitrap Index (OI) in the buffer area was higher com- tained from indoor-installed ovitraps: 23.5 to 17.4% in pared to that in the perimeter area. The results showed the perimeter area and 25 to 14.8% in the buffer area. that the buffer areas have more potential as breeding sites On the other hand, positive transovarial transmissions in of Aedes spp. mosquitoes. The distribution of Aedes spp. Aedes albopictus mosquitoes were all found in samples mosquitoes based on positive OI in Yogyakarta’s Adisu- cipto Airport was found evenly distributed in the sur- Table 1 Distribution of ovitrap installation in Adisucipto Airport rounding areas, with the highest number of positive OI of Yogyakarta found in the zone 4, the neighborhood 8 (Rukun Location Situation (+) Eggs OI (%) Tetangga/RT 8) of village of Maguwoharjo. OI of < 5% Indoor Outdoor Indoor Outdoor Indoor Outdoor shows that the distribution of Aedes spp. mosquitoes is least spread, while OI of 5–20% shows that the Aedes spp. Perimeter area 40 34 12 12 30 35.3 mosquitoes are moderately spread in the study area . Total number 74 24 32.4 OI of < 10% indicates that the area has no risk in the Buffer area 29 42 11 21 37.9 50 development of dengue outbreak, whereas OI of > 10% Total number 71 32 45.1 indicates that the area has the potential for developing Satoto et al. Environmental Health and Preventive Medicine (2018) 23:22 Page 4 of 7 Fig. 1 Distribution map of dengue virus and dengue cases in Adisucipto Airport Yogyakarta in every Zones. Four zones in perimeter area are cargo log (zone 1), terminal A (zone 2), office (zone 3), and terminal B (zone 4), while four areas in buffer area (—) are terminal B (zone 1), parking and public facilities (zone 2), neighborhood 7 (zone 3), and neighborhood 8 (zone 4). Buffer area has more potential as breeding sites of Aedes spp. mosquitoes. The distribution of Aedes spp. mosquitoes based on positive Ovitrap Index in Yogyakarta’s Adisucipto Airport was found evenly distributed in the area, positive eggs ovitraps, positive virus ovitraps Ae. aegypti, positive virus ovitraps Ae. albopictus, and positive virus ovitraps Ae. aegypti and Ae. albopictus, with the highest number of positive OI found in the zone 4, the neighborhood 8 (RT 8) of village of Maguwoharjo. Negative ovitraps and dengue patients (sufferers) distribution may also be observed dengue outbreak . In the area of Yogyakarta’s Adisu- dengue in the area of Adisucipto Airport of Yogyakarta. A cipto Airport, OI of 45.1% was found, which indicates similar study in Manado, Indonesia, also showed that the potential for developing dengue outbreak. TTI in Aedes aegypti mosquitoes is significantly higher The analysis of OI distribution resulted in z-score of − than that in Aedes albopictus mosquitoes . Previous 6.1 and p value of < 0.001 that indicates the tendency of research established that Aedes aegypti mosquitoes have a clustered OI distribution. Through identification by using major role in human dengue transmission . A TTI rate IHC method, the transovarial transmission was observed of 20% allows the maintenance of highly stable vertical in- higher in percentage in Aedes aegypti mosquitoes in the fection that persists for several generations . perimeter area compared to that in the buffer area. The Positive transovarial transmissions in Aedes aegypti percentage alone presumes that Aedes aegypti mosquitoes mosquitoes were more commonly detected in samples may have a more dominant role in the transmission of obtained from indoor-installed ovitraps in the perimeter Table 2 Analysis of transovarial transmission of Aedes spp. mosquitoes in Adisucipto Airport of Yogyakarta Location Immunohistochemistry (IHC) Transovarial transmission % transovarial transmission Ae. aegypti Ae. albopictus Ae. aegypti Ae. albopictus Ae. aegypti Ae. albopictus Perimeter area 40 18 8 3 20 16.7 Total number 58 11 18.9 Buffer area 59 56 12 9 20.3 16.1 Total number 115 21 18.3 Satoto et al. Environmental Health and Preventive Medicine (2018) 23:22 Page 5 of 7 Table 3 Serotypes of dengue virus in Aedes spp. mosquitoes in outdoor-installed ovitraps. Distribution of dengue virus in Adisucipto Airport of Yogyakarta the Adisucipto Airport of Yogyakarta was predominantly Location RT-PCR DENV found in zone 4 of the buffer area, the RT 8 of village of serotype Maguwoharjo. Dengue virus distribution tends to follow Aedes aegypti Aedes albopictus the distribution pattern of ovitraps. In both perimeter and Perimeter area buffer areas of the Adisucipto Airport, there were no den- 17a 12 DENV 2 gue cases found. This result may be due to lack of good 54a 2 DENV 2 and 3 host immunity, higher activities of humans in the airport so Buffer area that the mosquitoes were not able to bite very often , 110a 12 DENV 2 and 3 and low number of Aedes spp. mosquitoes in the Adisucp- 119a 5 DENV 2 and 3 tio Airport: 378 mosquitoes in ± 560,000 m perimeter and buffer areas. Other possible contributing factor is low TTI 132a 7 DENV 2 and 3 of dengue virus (18.9% in perimeter area and 18.3% in buf- 134a 4 DENV 2 and 3 fer area). These TTI values are considered low as the study 136a 2 DENV 2 was conducted in endemic area and in rainy season, during which dengue transmission is on its peak; therefore TTI area. The results suggest that Aedes aegypti mosquitoes values should exceed 30% . As described in Fig. 1,the tend to do oviposition indoor rather than outdoor. A shortest distance of dengue patients was 389 m, whereas study in three localities in Malaysia also showed that ovi- the farthest distance was 1050 m. traps were more likely to yield positive results if installed The analysis of dengue virus distribution was conducted indoor . using the nearest neighbor analysis and resulted in a Positive transovarial transmissions in Aedes albopictus z-score of − 2.0 and p value of 0.04 that indicates the ten- mosquitoes were all found in samples from dency of clustered distribution. The shortest distance of Fig. 2 Distribution map of dengue virus and dengue cases in Adisucipto Airport Yogyakarta. Four zones in perimeter area are cargo log (zone 1), terminal A (zone 2), office (Zone 3), and terminal B (zone 4), while four areas in buffer area are terminal B (zone 1), parking and public facilities (zone2), neighborhood 7 (zone 3), and neighborhood 8 (zone 4). One spot was positive in perimeter area for DENV-2 and one spot positive for DENV-2 and DENV-3, both of which were also positive for Ae. albopictus. One spot was positive in buffer area for DENV-2 and two spots were positive for DENV-2 and DENV-3, all of which were also positive for Ae. albopictus. There were two spots positive in buffer area for DENV-2, DENV-3, and Ae. aegypti Satoto et al. Environmental Health and Preventive Medicine (2018) 23:22 Page 6 of 7 positive ovitraps was 3.1 m, while the farthest distance RT-PCR: Reverse transcriptase-polymerase chain reaction; TTI: Transovarial Transmission Index; WHO: World Health Organization was 33 m with average distance of 15.2 m. Although no specific threshold values have been established for each Acknowledgements arbovirus, absence of severe dengue cases in Thailand was Deepest gratitude is directed towards Angkasa Pura II, Agricultural Quarantine, and Airport Security of Yogyakarta’s Adisucipto Airport, as well as noted when the density of Ae. aegypti eggs per ovitrap per towards the Port Health Quarantine of Yogyakarta who have been providing week was less than two . Moreover, despite using a dif- generous support. The authors would also like to acknowledge the ferent ovitrap, DENV transmission occurred in Taiwan Indonesian Ministry of Health for funding this study. Last but not the least, the authors would like to give appreciation to Dr. Ajib Diptyanusa for editing when the density of eggs per house (two ovitraps per the final manuscript. house) was around two . In determining transmission of dengue virus, TTI is important in showing that dengue Funding The funding body had no roles in the field survey, analysis, and virus from infected female mosquitoes may be spread into interpretation of data as well as in writing the manuscript. the ovarii and transmitted to the next generation, whereas OI correlates with mosquito population and represents Availability of data and materials true mosquito infestations in the area [11, 22]. Data sharing is not applicable to this article as no datasets were generated or analyzed during the current study. The study was a part of AL's thesis. The Dengue virus serotype examination was performed in data used in this article are not published elsewhere. dengue-positive Aedes spp. mosquito-colonized samples and in positive transovarial transmission samples, all of Authors’ contributions TBTS carried out the molecular genetic studies, conceived of the study, and which were coded in species and location: DENV-2 and participated in its design and coordination and in drafting the manuscript. DENV-3. Similar results were obtained in Bantul, AL carried out the field works and data analysis, while SDA participated in Indonesia, which showed the predominant serotypes of the surveillance. HKJ participated in the design of the study and performed the statistical analysis. BSW has provided assistance in designing and dengue virus in Aedes aegypti mosquitoes were DENV-3 reviewing the map. All authors have read and approved the final manuscript. (12 locations), followed by DENV-2 (3 locations), DEN-4 (1 location), and DENV-1 (0 location) . Studies con- Authors’ information TBTS is a member of Indonesian Entomological Association and is active ducted in Thailand  and Singapore  showed that in research in mosquito-borne diseases. AL and SDA are surveyors in DENV-2 was the predominant serotype found. In areas Port Quarantine. HKJ is a professor in Public Health. BSW is an expert in with high dengue endemicity, the predominant serotypes map drawing. were DENV-2 and DENV-3, while in areas with low Ethics approval and consent to participate dengue endemicity the prevalent serotypes were Ethical approval was obtained from the Medical and Health Research Ethics DENV-1 and DENV-2 . A similar study conducted Committee (MHREC), Faculty of Medicine Universitas Gadjah Mada, in 2007 to 2009 in Brazil reported that the highest num- recognized by FERCAP. ber of mosquito larvae found was Aedes aegypti (3417 Competing interests mosquitoes or 91%), followed by Aedes albopictus (336 The authors declare that they have no competing interests. mosquitoes or 9%), with detected serotypes of DENV-3 Aedes albopictus, DENV-2 Aedes aegypti, and DENV-2 Publisher’sNote and DENV-3 Aedes albopictus . Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. The study has several limitations. First, the study was conducted only once during rainy season, which would Author details have been better if performed simultaneously in other Center For Tropical Medicine, Faculty of Medicine, Universitas Gadjah Mada, Jl. Farmako Sekip Utara, Yogyakarta, Indonesia. Port Health Quarantine, season as well. Second, study area was limited only to Adisucipto Airport, Yogyakarta, Indonesia. Department of Public Health, areas open for public access, not including those areas Faculty of Medicine, Universitas Gadjah Mada, Yogyakarta, Indonesia. that belonged to the Air Force and not open for public. Department of Geographic Science, Faculty of Geography, Universitas Gadjah Mada, Yogyakarta, Indonesia. Conclusion Received: 12 August 2017 Accepted: 13 May 2018 The study shows that buffer areas of Adisucipto Airport of Yogyakarta have higher risk as breeding sites for Aedes References spp. mosquitoes, predominantly DENV-2 and DENV-3 se- 1. World Health Organization. Dengue: guidelines for diagnosis, treatment, rotypes. OI of 45.1 indicates that the area has the potential prevention and control. Geneva: World Health Organization; 2009. for developing dengue outbreak. 2. Wilson ME. The traveller and emerging infections: sentinel, courier, transmitter. J Appl Microbiol. 2003;94 Suppl:1S–11S. 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