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 Epidemiology and Society Health Review| ESHR 
Vol. 3, No. 2, 2021, pp. 1-9 ISSN 2656-6052 (online) | 2656-1107 (print) 
 
 

      10.26555/eshr.v3i2.3719  

 
 
1 

 
 

  

Research Article 
 
Entomological Index and Insecticide Susceptibility Status 
In Dengue-Endemic Areas Yogyakarta 
 
Fardhiasih Dwi Astuti1* and Arlina Azka1 
1 Faculty of Public Health, Ahmad Dahlan University, Yogyakarta, Indonesia 
 
* Correspondence: fardhiasih.dwiastuti@ikm.uad.ac.id. Phone: +6281328299534 
 
Received 21 February 2021; Accepted 30 July 2021; Published 31 July 2021  
 

ABSTRACT 

Backgrounds: Dengue Hemorrhagic Fever (DHF) is a disease that receives special 
attention because of causing outbreaks in some countries, including Indonesia. The 
problems that often emerge on the DHF Control Program are the high vector density (Aedes 
aegypti) and the vector resistance resulting from continuous insecticide use. This study 
describes the entomological index and susceptibility status of Aedes aegypti against 
malathion and permethrin insecticides in Sorosutan, Umbulharjo, Yogyakarta. 
Methods: This study used a descriptive observational method with a cross-sectional 
design. An entomological survey was done at 354 houses in Sorosutan, which was 
randomly selected. The sample of Aedes aegypti was obtained through the larval collection 
and ovitrap installation in 100 places. Susceptibility tests performed using the bioassay 
method with impregnated paper were based on the WHO standard. This study was 
conducted from December 2018 – February 2019. The data were analyzed using univariate 
analysis 
Results: The entomological survey in Sorosutan showed the House Index value was 
35.03%; Container Index was 16.68%; Breteau Index was 46.33; Density Figure was 5.00, 
and Larva Free Rate was 64.97%; meaning that Sorosutan had a high level of vector 
density. So, the risk of DHF transmission was high. The population of Aedes aegypti in 
Sorosutan has been tolerant against Malathion, with 87.83% mosquito mortality. 
Conclusion: Sorosutan was an area with high DHF transmission risk. Aedes aegypti 
population in Sorosutan has been tolerant against Malathion.  

Keywords: Entomological index; Susceptibility status; Aedes aegypti; Malathion 

INTRODUCTION 

Dengue Hemorrhagic Fever (DHF) is a disease that receives concern globally because it 
continues to cause an outbreak in several countries. The incidence of DHF has increased 
rapidly worldwide in recent decades. It was estimated that as many as 390 million people per 
year were infected with DHF, of which 96 million people have clinical manifestations with a 
relatively high level of disease severity. In addition, as many as 3.9 billion people in 128 
countries are at risk of being infected with the dengue virus (1). 



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In Indonesia, dengue has a moderately severe impact socially and economically. Since the 
discovery of the first case in 1968, there has been an increase in dengue cases and endemic 
areas of DHF. The high number of dengue cases in Indonesia is related to high population 
mobility, uncontrol urban growth, climate change, density changes, population distribution, low 
public awareness to maintain environmental sanitation, and other epidemiological factors that 
still require further research (2). DHF cases in Indonesia are spread across cities in Indonesia, 
including Jakarta, Surabaya, Medan, Bandung, and Yogyakarta (3,4). 

Yogyakarta City is an endemic area of DHF in Daerah Istimewa Yogyakarta (DIY). The highest 
incidence of dengue fever in this city in 2017 was in Sorosutan village, with an Incidence Rate 
of 20.6 per 100,000 population (5). Sorosutan village has the highest population compared to 
44 other villages in Yogyakarta City. With this condition, there is a potential for an increased 
risk of dengue transmission in the area. 

Efforts to treat DHF so far are only based on the symptoms of the disease. However, in a 
situation where there is no specific dengue medicine, it is necessary to take effective 
countermeasures to reduce the incidence of dengue fever so that it does not continue to 
increase. Vector control is the primary prevention effort that has been and is still being carried 
out by the government to break the chain of transmission of dengue fever (6). In addition, 
monitoring Aedes sp larvae and the breeding place is also continuously carried out. 

Vector density can be an indicator of the success of a DHF control program. The density of 
Aedes sp can be identified using the larva free rate (LFR), House Index (HI), Container Index 
(CI), Breteau Index (BI), and Density Figure (DF). The density Figure is a combination of HI, 
CI, and BI (7). Besides Mosquito Nest Eradication or PSN in Indonesia, chemical control is 
also carried out by applying fogging and household insecticides. Malathion is a chemical for 
fogging that has been used in the Dengue Hemorrhagic Fever eradication program in 
Indonesia since 1973. This insecticide is one of the safe and cheap ones widely used in 
households (8). The use of Malathion as a fogging solution in Yogyakarta has been substituted 
with cypermethrin since 2016. DHF control by fogging is only carried out if cases are found 
and transmission occurs in the area (9). Permethrin is one of the chemicals contained in over-
the-counter household insecticides (10). The danger of using chemicals continuously can 
cause resistance to the dengue vector. Vectors that have been resistant when they reproduce 
will produce offspring that have resistant genes. The higher the frequency of individual 
resistant vectors, the rate of resistant development will be faster. Accordingly, the population 
will be dominated by resistant vectors. Insects such as Aedes aegypti can maintain and pass 
resistance traits to their offspring for a long time (11,12) 

Resistance to Malathion has been reported in several areas in Indonesia, including 
Simbangkulon Village, Buaran District, West Kedungwuni Village, Kedungwuni District, and 
Karangsari Village, Karang Anyar District, Pekalongan District (13). In the Special Region of 
Yogyakarta (DIY), Aedes aegypti resistance to Malathion was reported in Panggungharjo 
Village, Bantul Regency, Plososkuning Minomartani, and in several hamlets in Gamping 
District, Sleman District (14). Malathion as a fogging chemical has not been followed by 
evaluating sensitivity to Aedes Aegypty in the Sorosutan area. This study aimed to determine 
the entomological index and susceptibility status of Aedes aegypti to malathion insecticides in 
Sorosutan Village, Umbulharjo District, Yogyakarta City. 



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METHOD 

This research was a descriptive observational study. An entomological survey was conducted 
in 354 houses in Sorosutan Village. Mosquito samples were collected by collecting larvae and 
installing ovitraps in 100 purposively selected houses. House used for placing ovitrap should 
fulfill criterias: have a positive larval house, have 100 m distance previous ovitrap installed, 
and a house with poor lighting. Mosquito breeding was carried out at the Test Animal 
Maintenance Laboratory, Universita Ahmad Dahlan. Vulnerability testing was carried out using 
impregnated paper according to WHO standards. Impregnated paper with 5% malathion 
content was obtained from Universiti Sains Malaysia (USM), Penang, Malaysia, a WHO 
Collaborating Centre. 

Mosquito for testing pruposes was prepared by incubating Aedes aegypty eggs from ovitrap 
installation. The hatched larvae were reared by feeding chicken liver powder, and water was 
distorted every two days. Larval rearing was carried out until they became adults of the first 
generation (F1). Mosquitoes used as samples for susceptibility testing were Aedes aegypti 
adult females aged 3-5 days with sugar-water satiety conditions. 

The susceptibility test was carried out on treatment tubes containing impregnated paper and 
control (without impregnated paper). Each tube was filled with 25 mosquitoes exposed to 
impregnated paper for one hour. Then, the mosquitoes were transferred to the storage 
holding, observed the number of mosquitoes that fainted, and the number of deaths recorded 
after 24 hours. The test was carried out three times on each 5% impregnated paper malathion. 
Vulnerability testing was carried out at the Entomology Laboratory of Universitas Ahmad 
Dahlan. Vulnerability status was obtained from the number of mosquito deaths which were 
then categorized as vulnerable (98% – 100%), tolerant (80% – 97%), and resistant (< 80%) 
(15). The research was conducted in December 2018 – February 2019. 

RESULTS 

Sorosutan Village entomological index 
The entomological index was obtained from an entomological survey in 18 RWs in the 
Sorosutan Village, Yogyakarta. 

Table 1. Sorosutan Village Entomology Index December 2018 – January 2019 
 

No. Entomology Index Results 
1 House Index (HI) 35.03% 
2 Container Index (CI) 16.68% 
3 Breteau Index (BI) 46.33 
4 Density Figure (DF) 5.00 
5 Larva Free Rate (LFR) 64.97% 

 
Table 1 shows that the HI, CI, and BI values in Sorosutan Village are pretty high, namely the 
HI of 35.03%, CI of 16.68%, and BI of 46.33. The combination of the three indicators produces 
a DF value of 5.00. In addition, the larva-free rate (ABJ) obtained is relatively low, namely 
64.97%. 
 



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Status of Aedes aegypti susceptibility to Malathion  
The following are the susceptibility test results to the malathion insecticide carried out on the 
Aedes aegypti mosquito from the Sorosutan Village area. Table 2 shows that the population 
of Aedes aegypti in Sorosutan Village is tolerant to malathion insecticide with an average 
mortality of 87.83%. 

Table 2. Vulnerability Status of Aedes aegypti Population in Sorosutan Village to 
Malathion and Permethrin Insecticides 

 

Insecticide Average Mosquito Mortality 
(%) 

Vulnerability 
Status 

Malathion 87.83 Tolerant 
  

DISCUSSION  

Based on the results of the entomological survey, the inspected houses and containers can 
be calculated values that are indicators of vector density and the risk of dengue transmission 
in the area, namely the House Index (HI), Container Index (CI), Breteau Index (BI), Density 
Figure ( DF), and Larvae Free Rate (LFR). The HI value is 35.03%, and the CI is 16.68%. HI, 
values > 5% and CI > 10% indicate that the Sorosutan area has a high risk of DHF 
transmission. Meanwhile, based on the BI value obtained, 46.33, where the value is not more 
than 50, the transmission of DHF in the Sorosutan area is not included in the high category 
(16). Based on the DF value, which is 5, it was indicated that the risk of DHF transmission in 
the Sorosutan area is in the moderate category. The WHO stated that the HI value > 5% and/or 
BI > 20 for each region indicates that the region is sensitive to dengue fever. Accordingly, 
Sorosutan was categorized as a sensitive area to dengue fever (17). 

This result aligns with a study in the Mamuju region, Sulawesi, which shows a larva-free rate 
of 62.7% (July – August 2015) (18). The larva-free rate nationally for 2016-2019 showed 
67.6%, 46.6%, 31.5% and 79.2%, respectively. This shows that areas in Indonesia are at risk 
of dengue transmission. From 2010 to 2019, there was an increase in the area of dengue 
cases in Indonesia. In 2019, 93.58% of the area in Indonesia was infected with dengue fever.  
While in DIY during 2019, the incidence rate was more than 49 per 100,000 population (85.9 
per 100,000 population) (19). 

Poor entomological indicators lead to a high risk of dengue transmission. This is because 
knowledge, behavior, and community participation to be directly involved in Mosquito Nest 
Eradication (PSN) activities are still inadequate (20,21). This can be seen from the results of 
the larva-free rate (LFR) in Sorosutan of 64.97%, which was still far from the national target 
according to the Indonesian Ministry of Health (95%). The low larva-free rate indicates that 
the PSN program in Sorosutan was still lacking. This is in line with research that states a 
relationship between PSN's actions and the presence of larvae at Pulang Pisau Port with a p-
value of 0.000. Respondents who have bad actions have a 3.89 times greater risk of larvae 
than respondents who have good actions (22). Some studies have shown a relationship 
between mosquito density and high dengue cases (23,24). 

Community participation is needed to implement vector control mostly influenced by the 
community's knowledge, attitudes, and behavior (21). The implementation of vector control 
can be carried out through environmental management called integrated vector management 



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(IVM). IVM combines mosquito breeding site elimination and chemicals by administering 
larvicides at mosquito breeding sites and fogging to kill adult mosquitoes that are implemented 
simultaneously (23). IVM was proven by a study in Makassar that reduced the incidence of 
dengue (24).   

Based on the susceptibility test to malathion insecticide, it was found that the population of 
Aedes aegypti in the Sorosutan village area was in the tolerant category. Malathion is an 
organophosphate insecticide. The way these insecticide works is by inhibiting the enzyme 
cholinesterase (AChE) in nerve cells. This enzyme works to hydrolyze acetylcholine into 
acetate, and choline—acetylcholine functions as a neurotransmitter in the synaptic cleft. When 
the organophosphate is sprayed on the target organism, the AChE enzyme cannot work 
normally. Organophosphates phosphorylate the enzyme into a stable component form. So 
that acetylcholine cannot be decomposed in the postsynaptic (25). The research results in 
Plosokuning Yogyakarta showed that Aedes aegypti in the area was already resistant, 
increasing the esterase enzyme activity. Esterase enzymes detoxify organophosphates, 
carbamates, and pyrethroid synthesis by hydrolyzing ester bonds and binding pesticides to 
the active esterase site (26).  

Resistance can arise due to the use of chemicals continuously for a long time and be given to 
the next generations of these mosquitoes. We found that in the household in Sorosutan, most 
of them applied the insecticide daily and continuously. Aedes aegypti is able to be given the 
resistant traits to their offspring for a long time (11). A study in the United States showed that 
the population of Ae. albopictus in Florida and New Jersey were found to be resistant to 
Malathion. The study also found significant differences in the activity of detoxification enzymes 
which suggest a metabolic-based resistance mechanism. Malathion-resistant populations 
have increased esterase and glutathione S-transferase enzymes (27). The presence of 
esterase enzyme activity in the mosquito population will resist other insecticides with ester 
groups. Therefore, in areas with mosquito populations resistant to Malathion, it is advisable to 
choose an active ingredient not from the organophosphate group and has a different 
mechanism of action from Malathion (13). 

The results of this study are in line with research conducted by Sukmawati that the Aedes 
aegypti population originating from Makassar City is tolerant to 5% malathion with an average 
mortality of 87% (28). Tolerance status can become resistant to Malathion if the insecticide is 
used continuously without rotation. The area reported to be resistant to Malathion is 
Panggungharjo Village, Bantul, with a 0% mortality percentage (100% resistance) (14). In 
Tomohon City with 0% mosquito mortality (29). In Semarang, resistance was reported at 
Tanjung Emas Port with mosquito mortality in the buffer area of 13% and perimeter of 20% 
(30). In Pekalongan District, Central Java, the mortality of the test mosquitoes ranged from 
13.75-25% (14). East Jakarta has 53% mosquito mortality, West Jakarta 75%, and South 
Jakarta 53% (31). In Banten province, including South Tangerang, mosquito mortality was 
73.9%, Serang was 46.9%, and Cilegon was 60.2% (32). In Ambon City, Maluku Province, 
resistance was reported in the Yos Sudarso Port area and the Nusantara Fisheries Port with 
20% mosquito mortality, at Pattimura Airport with 16% mosquito mortality in the perimeter area 
and 20% in the buffer area (33).  

Resistance to a type of insecticide is generally based on three mechanisms: a decrease in 
target site sensitivity, changes in the cuticle layer that can reduce the penetration of 



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insecticidal compounds into the insect's body, and an increase in detoxification enzymes. The 
mechanism of resistance can be determined by carrying out biochemical tests or molecular 
tests on vectors. Biochemical test to see the activity of enzymes that detoxify insecticides 
(metabolic resistance) as the basis for the occurrence of insect resistance to insecticides. 
Meanwhile, molecular tests were carried out to detect insect resistance to insecticides by 
finding the point mutation of the voltage-gated sodium channel (VGSC) gene as the target site 
of the insecticide workplace. The research results in Palembang showed that based on 
biochemical tests, there is no increase in the level of insecticide detoxifying enzymes that 
neutralize synthetic pyrethroid insecticides. Resistance is suspected due to a decrease in the 
sensitivity of the target site. This is evidenced by molecular tests showing mutations in the 
VGSC gene in Aedes aegypti (34). 

The Yogyakarta City Government has substituted Malathion as an active insecticide ingredient 
for fogging with cypermethrin since 2016. This step was an effort to prevent further resistance 
from occurring. However, the use of cypermethrin without Aedes susceptibility testing is not 
appropriate because resistance has been reported in the Yogyakarta city area to cypermethrin 
and permethrin in 2010 (35). Several regions have stopped using malathion insecticide 
because resistance has occurred; after 5 - 10 years of retesting, the results still show 
resistance to the insecticide (36). Cypermethrin is a synthetic pyrethroid insecticide like 
permethrin. Permethrin is a third-generation pyrethroid, and cypermethrin is a fourth-
generation pyrethroid. In areas where resistance to permethrin is found, replacing (rotate) with 
other insecticides that work differently from pyrethroids is recommended. This method can 
prevent or reduce permethrin resistance to a higher level and not spread to other areas in 
Indonesia (37). If cypermethrin is used continuously, it can pose a threat of resistance in the 
future. Efforts that can be made to reduce the potential for insecticide resistance in an area 
are by rotating the active ingredients of the insecticides used. Changes in the type and 
workings of insecticides for vector control must be carried out within a maximum of 2 – 3 years 
or 4 – 6 times of application. However, the change can be accelerated according to monitoring 
the vulnerability status (8). 

In addition to organophosphate and pyrethroid insecticides, carbamate insecticides can also 
be used for vector control by misting (8). However, the mechanism of toxicity of carbamate 
insecticides is the same as that of organophosphates, namely by inhibiting the action of the 
acetylcholinesterase enzyme so that it undergoes carbamylation. Carbamates work by binding 
to the enzyme acetylcholinesterase, which functions to hydrolyze acetylcholine. The binding 
of the acetylcholinesterase enzyme causes a buildup of acetylcholine which causes the nerves 
to be continuously stimulated, causing tremors and other uncontrolled movements (9). This 
means that carbamate insecticides will not be effective when used on Aedes aegypti 
populations resistant to organophosphates due to increased acetylcholinesterase enzymes. 
Testing the sensitivity of the acetylcholinesterase enzyme in the biochemical microassay 
method using propoxur (a carbamate insecticide) to help detect the activity of detoxification 
enzymes involved in the resistance mechanism of mosquito larvae temephos (an 
organophosphate insecticide). A study showed that decreased acetylcholinesterase sensitivity 
also indicated the emergence of resistance to organophosphates and carbamates in the 
Aedes albopictus population from Selangor Malaysia (38).  

As part of an effort to reduce the incidence of Dengue Hemorrhagic Fever, insecticides 
(chemical control) should be an option to control mosquito vectors. Environmental-based 



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control with PSN is the main activity that must always be carried out to suppress vector 
populations. The use of insecticides cannot continue to be a foundation because it has an 
unfavorable impact on the environment. Therefore, environmental-based prevention and 
control efforts are the main focus, and the community's active role is needed. 

CONCLUSION 

Sorosutan village, Yogyakarta City, has a high risk of transmission of Dengue Hemorrhagic 
Fever (DHF). The population of Aedes aegypti in the Sorosutan Village area was tolerant to 
malathion insecticides, with mosquito mortality of 87.83%. Mosquito nests by being 
independent larvae monitor in their respective neighborhoods and consistently applying 
3M were the three Ms stands for Menutup, Menguras, and Mengubur, meaning covering water 
containers, cleaning water containers, and burying discarded containers to avoid DHF. The 
main focus of dengue control is on environmental management by eliminating the breeding 
place for Aedes sp. 

Authors' contribution 

FDA prepared the manuscript draft and research funding. AA was responsible for data 
collection and reviewed the manuscript.  

Acknowledgment 

We thank Ahmad Dahlan University for the support of laboratory facilities in facilitating this 
research. 

Conflict of interest 

There is no conflict of interest in this research.  

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