The incidence of malaria in South Kalimantan province has experienced a very significant decline in recent years. However, in several districts, including Tanah Bumbu, malaria cases were still found, especially in remote areas. Kusan Hulu sub-district is one of the districts that still have malaria-red areas. The research village is a remote area located in the Meratus mountain plain and included in a protected forest area. Therefore road infrastructure is still an obstacle to access to villages in this region. Conditions like this are one of the complications in eradicating malaria [20, 21].
The incidence of malaria usually increases at the end of the rainy season. Even so, malaria cases always occur every month in this study area. Other studies have shown that although malaria cases increased significantly in May, October to July, there are always case reports every month [22]. This research was conducted in September 2020 which is the beginning of the rainy season. The prevalence of malaria is 18.1% at the beginning of the rainy season, indicating that malaria transmission continues throughout the year in this area. The reason is that it still rains, even though it is in the dry season. High sun exposure causes a high intensity of evaporation so that there are always active clouds. The average length of exposure ranges from 1.2 hours to 7 hours in September 2020. The average rainfall intensity ranges from 0.9–16 mm, with the number of rainy days ranging from 5–28 days/month. The average minimum temperature during the dry season is 22.7oC − 24.7oC and the average maximum temperature is 30.5oC − 32.9oC [23]. This condition is a good condition for the breeding of Anopheles sp [24].
Research in Guangdong, China showed that the temperature threshold associated with malaria transmission is unclear [25], yet, Kim et al. showed that malaria transmission changes slightly above 24°C in Korea. This may be due to the relatively shorter temperature range in sub-tropical [26]. In contrast to Indonesia, which has a tropical climate with 2 seasons, where the average temperature is relatively hot. It is known that the optimal development of the malaria parasite at temperatures between 25–30oC. Research also shows that at hotter temperatures, P. falciparum reproduction is more optimal than P.vivax. P.falciparum undergoes the entire life cycle in a shorter time at temperatures of 28–30°C. Heat favors the development of P. falciparum and may have a significant effect on mosquito infection rates and parasite density. Plasmodium vivax completes growth and development in a wider range from 15 to 30°C and may therefore be less sensitive to temperatures [25].
The relationship between malaria transmission and temperature is still widely debated. Several studies using the Martens 3, Bayoh-Mordecai, and Bayoh-Lunde models show that malaria transmission is more efficient at 25oC, but based on the Martens 2 and Bayoh Ermert model, malaria cases were more prevalent in areas with temperatures approaching 27oC. The Martens 1 model has a peak temperature of 20.4oC and Bayoh-Parham at 26.3oC [27]. This explains why in high mountain areas with temperatures below 18oC, malaria transmission is rare and almost doesn’t exist. However, if the temperature increases, there will be an increase in transmission. Liu et al. showed that an increase in temperature of 5oC − 10oC would result in a 22% increase in malaria cases within 4 weeks [28].
The number of rainy days in the rainy season in South Kalimantan ranges from 20 to 30 days/month within light (50 mm) to heavy (100 mm) and very heavy (> 150 mm) rainfall. The average humidity in this area is between 80–90% [23]. Rain can form new puddles that can become breeding places for Anopheles mosquitoes, this will increase the density of vector mosquitoes. This has led to an increase in malaria cases during the rainy season and beyond. However, very heavy and extreme rainfall do not always cause an increase in the breeding place for Anopheles mosquitoes. Research shows that in areas with very heavy or extreme rainfall, mosquito eggs and larvae are washed away and wasted, disrupting the development cycle [29].
Plasmodium falciparum was the most common species in this study, with about 47.37% of all malaria-positive, followed by P. vivax and mixed infections. This study has similarities with the research of Nath and Mwchahary in India which showed that the prevalence of P. falciparum was still high in forest and non-forest areas [8]. The high of P. falciparum infection indicates a risk of serious complications. However, falciparum malaria can be treated quickly using an artemisinin regimen. In contrast to P. vivax infection, which is usually more difficult to treat because it has a hypnozoite stage in the liver [30]. To kill this hypnozoite stage, treatment with Primakuin is required for a longer oral administration time and potentially causes low drug adherence rates. P.vivax also can transmit malaria despite the low parasite density in the blood. Mixed infections (P. vivax and P. falciparum) that are persistent and usually asymptomatic are common in areas within low malaria transmission. Infections with low-density parasitemia can progress to high-density infections at other times, and this tends to maintain the level of endemicity [31, 32, 33].
Most of the participants with positive malaria parasites in this study were asymptomatic. It is probably a consequence of acquired immunity due to the high transmission intensity in this area. People with asymptomatic malaria have the potential to spread and sustain transmission if they are not detected and given treatment. This research was conducted at the beginning of the rainy season, which theoretically is not the peak of malaria transmission. It is possible to find more cases during the peak season of transmission at the end of the rainy season. Therefore, it is necessary to carry out regular surveillance to detect and monitor asymptomatic malaria to prevent wider transmission [31, 32].
Batu Bulan and Batu Paha Villages are the remote villages in Tanah Bumbu Regency. These two villages are on the border with Banjar Regency. Most of the people who live in this village are Banjarese. Another tribe that also exists is the Dayak tribe, although the numbers are small. They have lived side by side for a long time, making physical ethnic separation extremely difficult. Ethnically, there is no significant difference in the incidence of malaria between the two tribes. Apart from being mixed, the factor of the same occupation as forest workers was the reason there was no significant difference in the prevalence of malaria based on ethnicity. The study by Achidi et al. in Cameroon shows that there are differences in the number of parasitemia in 3 different tribes even though they live in the same area. This difference is due to a genetic variation in the immune response to a pathogen [34]. Some tribes have a certain susceptibility to malaria, while others may be more resistant to infection. However, the research also shows that this difference is due more to pathogenic factors than to immune factors [35].
Activities in the forest are one of the risk factors for malaria transmission in The Kusan Hulu District. Forest workers were 4,332 times more likely to be infected with malaria through the bite of Anopheles sp. The types of work they do are gold miners and woodcutters. Gold mining in these forest areas starts in the morning around 04.00. This is the reason why gold miners are more frequently infected with malaria. Similarly, Sanford et al. showed that working in the forest is a risk factor for malaria transmission in Cambodia 2 to 3 times. This research also shows that living in a village that is in the forest has a high probability of contracting malaria (aOR 12.47) [2]. In Asia-Pacific, forest activities such as agriculture, logging, and gold mining at high risk for exposure to malaria. Workers in these forest areas tend to show patterns of mobility between endemic and non-endemic areas which can contribute to sustaining transmission and even lead to new cases of malaria that have previously been eliminated [36].
The forest ecosystem provides a suitable habitat for the development of the malaria mosquito vector. Environmental factors including climate, vegetation, and the availability of breeding places are important factors in malaria transmission. The mosquito species that is often found in the forest is Anopheles balabacencis. This species is the main vector of P.knowlesi transmission in Malaysian Borneo [37]. Malaria vectors found in South Kalimantan based on research by Harbach et al. in 1987 are An. balabacencis and An. leucosphyrus [38]. Research by Indriyati et al., In Siayuh village, Kotabaru district, which is adjacent to the Tanah Bumbu district, shows that the most common species of Anopheles are An. Tessellatus, An.vagus, An. Kochi and An. hyrcanus gr. Anopheles tesselatus and An.vagus are mosquitoes that are potential vectors of vivax malaria, which are commonly found near livestock sheds. Meanwhile, in the gold mining area, there are many species of An. maculatus and An. leucosphyrus [39]. This is also similar to the research of Edward et al., which shows that An. maculatus is the most dominant vector in the gold mining area on the border of Thailand and Myanmar [40].
Vector species and their biting behavior are important factors in malaria transmission in some areas with high insecticide-treated bed nets coverage [40]. Some areas show that vector biting behavior in the early evening or at dawn affects the incidence of malaria despite the very high use of bed nets. The main vector with its characteristics and behavior in an area must be known so that prevention can be carried out appropriately and effectively. The habit of biting vectors such as indoors or outdoors, the time of biting, and their preference for animal or human blood will affect the transmission of malaria in an area [41, 42, 43].
The structure of the house has been proven to be one of the factors that facilitate the transmission of malaria [41, 42, 43]. The results of this study indicate that almost all residents own houses with wooden walls and tin roofs. Only a small proportion of the population has a plastic roof. The population who experienced malaria infection in this study had a partially open house. The malaria vector biting outdoors will freely enter this open house and obscure the indoor/outdoor bite difference. People are more easily exposed to mosquito bites if they live in a shack or temporary house where the walls are mostly open and the roof is not permanent [40]. A study in Vietnam showed that wooden or bamboo houses had a higher risk than permanent houses in the same village (odds ratio 4.18 Cl 1.45–12.10) [6]. It is easier for mosquitoes to enter houses with wooden or bamboo walls through open gaps. Arranging bamboo or wood in an overlapping or layered manner can reduce the possibility of mosquitoes entering the house. The use of insecticide-treated mosquito nets in the house that is not tight can reduce the bite of malaria vector [44]. Similar observations in Gambia and Ethiopia show that houses equipped with ceilings and mosquito nets can reduce the density of mosquitoes inside the house [45, 46, 47].
The existence of cattle sheds around the house or inside the house is one of the risk factors for malaria transmission [48]. In this study, residents who had cattle sheds around their houses were more likely to be exposed to malaria (OR = 6.292) compared to residents who did not have cattle sheds. The livestock that kept in this village is chickens and goats with a cage distance from the house ranging from 2 to 3 meters. Having cattle sheds can lead to an increase in vector density around the house. This risk will increase if the cage is inside the house [49]. It shows that livestock can attract Anopheles, especially those that are zoophilic. The presence of livestock can also reduce Anopheles mosquito bites in the home, but not all studies support this result. The impact of livestock on malaria and vector density is complex. Some studies show that livestock provides zooprophilic protection while other studies show that livestock increases the risk of [50.51].
The research of Hasyim et al. shows that there is a positive relationship between keeping animals in the house and the prevalence of malaria (AOR = 2.809). The explanation for this result is that the presence of livestock attracts the population of mosquitoes that are vectors of Plasmodium into the house, thereby increasing exposure to humans through zoopotentiation. Zoopotentiation can also occur if physical disturbance caused by animals (e.g., standing water, hoof prints, watering sites) increases the potential for larval habitat and therefore increases vector density near houses [48]. Increased abundance of goats or sheep has been shown to increase Anopheles mosquito abundances. within a 20 m radius around Kenyan households. Each additional goat or sheep increases local malaria vector abundance [52].
Limitation of Research
The weakness of this study is that data collection was only carried out once in September 2020, ifthere is a prolongation time this time is extended it may be possible to obtain a more larger number of participants. Besides, access to the research area is tremendously difficult, accompanied by grossly inadequate infrastructure, making the process of storing blood sampling difficult. This study also did not measure temperature and rainfall in real-time, only taking data from the Meteorology and Geophysics Agency. Entomological measurements were also not carried out, due to the limitations of the researchers. However, this study can be a preliminary study to see the relationship of malaria with density, behavior, and habits, as well as the presence or absence of Plasmodium in the mosquito vector body.
Recommendations
The results of this study indicate the large potential for malaria transmission in remote forest areas with people working in the forest as the main occupation. People who live in villages in the middle of the forest with houses that are structurally open and uninhabitable leave them unprotected from mosquito bites. The existence of livestock sheds increases the risk of malaria infection because animals can act as vector attractants. All of these factors contribute to maintaining transmission through undetected infection. Surveillance in this remote area is tremendously difficult to carry out due to difficult road access, lack of lighting with electricity, and long distances from public health centers. By knowing the risk factors and their barriers, a more precise and effective malaria management program can be planned for this area. Intervention efforts such as reducing the reservoir or breeding place of Anopheles sp. in gold mine excavations, routine screening, and mass drug administration based on the screening results can help reduce malaria transmission. Expanding the usage of insecticide-treated mosquito nets to the population and replacing them regularly can be done, especially for houses that are not tight and whose roofs that made of plastic. Spraying houses with tight walls, especially at resting places for mosquitoes in the house, avoiding keeping animals in the house, and keeping livestock away from the house can help reduce the likelihood of mosquito bites in humans. The formation of malaria volunteers who are tasked with conducting counseling and screening in remote villages can also be an alternative in the management of malaria eradication planning so that the goal of malaria-free Indonesia by 2030 can be achieved.