TropicalMed, Vol. 7, Pages 392: Pattern of Aedes aegypti and Aedes albopictus Associated with Human Exposure to Dengue Virus in Kinshasa, the Democratic Republic of the Congo

1. IntroductionDengue is among the most common febrile mosquito-borne diseases (MBD) in the world [1]. The distribution pattern of dengue infections overlaps with the geographical distribution of its competent mosquito vector species. Dengue, similar to malaria, is involved in significant morbidity and mortality rates, with an adverse socioeconomic impact in the tropics and sub-tropics [1,2]. The clinical feature of the majority of mosquito-borne viral diseases (MBVD), such as dengue, is indistinguishable from a wide range of parasitic, bacterial, and other viral febrile illnesses due to limited diagnostic tools for use in most resource-constrained settings and the similarities of their clinical symptoms [3,4]. These facts lead to misdiagnoses, and then overuse of empirical malaria and antibacterial drugs as the morbidity and mortality burden of MBVD are often underestimated, particularly in developing countries [5]. The lack or limited availability of registered vaccines and the absence of curative treatment for the majority of MBVD hamper their control. The prevention based on integrated vector control and vigorous surveillance for the early detection of MBVD can reduce the risk of outbreak occurrence [6,7]. Moreover, the public health impact of MBVD is often esteemed only during an outbreak, and surveillance is not set up during the interepidemic period. However, studies have documented the circulation of MBVD in interepidemic periods [8,9].The outbreaks of MBVDs occur periodically across the world and tend to become progressively endemic in most of the well-known malaria endemic regions where their principal vector, Aedes aegypti, and Aedes albopictus coexist [10,11]. The global epidemiological standing over time identified the Democratic Republic of the Congo (DRC) as a country in which MBVDs, such as dengue, are an emerging or re-emerging disease. Dengue virus has been present in many provinces of the DRC for many decades with increased activity in recent years [12]. The recent report of dengue fever occurred during the chikungunya outbreak in 2012 in Kinshasa and later in 2016 [13,14]. The four serotypes of dengue have been documented in the DRC [15,16].The Aedes aegypti is the main urban vector for arboviruses such as dengue, yellow fever, chikungunya, and Zika. Except for yellow fever, the Asian native mosquito Ae. albopictus, which has invaded countries all over the world, is another competent vector for the transmission of these MBVDs [17]. The bio-ecology of these vectors is closely linked to climatic conditions (tropical and subtropical); environmental factors, such as the multiple natural or artificial water courses or containers; lack of proper waste management; and anthropogenic activities [18,19]. These conditions and factors are present in sub-Saharan Africa and lead to multiple MBVD outbreak occurrences. In urban areas, both species are mostly bred in uncovered domestic water storage units or any discarded container holding water. Moreover, in rural or forest areas, they are commonly bred in tree holes. The female adult mosquito is a blood-feeding insect that bites human during the daytime and, once infected, can successfully transmit and spread viruses [20,21]. In recent years, Ae. albopictus has been established in many places in Kinshasa [22,23,24] and is spreading to other provinces. It was recently documented in Tshuapa, a region located about 770 km from Kinshasa [25]. Therefore, both competent vectors of dengue, Ae. aegypti, and Ae. albopictus are present in the DRC. Little is known about their spatial distribution pattern and role in the spread of different MBVDs such as dengue in the DRC, which has recently experienced multiple chikungunya and yellow fever outbreaks [13,26,27,28].Dengue is an MBVD that has rapidly spread to all regions of the world in recent years. Today, almost half of the global population is at risk of dengue [1]. The clinical signs and symptoms include fever, joint pain, muscle pain, retro-orbital pain, and rash. Sometimes, the patients can present severe hemorrhagic disease and dengue shock syndrome, as well as respiratory and gastrointestinal manifestations [29]. The diagnosis of dengue infection can be performed serologically by enzyme-linked immunosorbent assays (ELISA), which may confirm a recent or past infection based on the presence of IgM or IgG antibodies. The viral ribonucleic acid detection by reverse transcriptase–polymerase chain reaction (RT–PCR) remains the gold standard. However, these expensive and sophisticated methods require appropriate equipment and experienced staff. The choice of the method to use should consider the time of patient presentation. RDT (rapid diagnostic test) dengue remains the convenient first choice in dengue-endemic regions and locations without adequate laboratory facilities [1,30]. The recent global spread of dengue has implied an urgent need for accurate, not time-consuming, and low-cost disease diagnostic methods such as RDT that could be easy to use even in resource-limited settlements [31], such as the DRC.

There is an important need to conduct a local investigation to gain insight into the extent of dengue in a country such as the DRC. The better identification of risk areas can rationally assist healthcare authorities to prioritize more efforts of the control activities at higher risk exposure areas. The primary objective of the current study was to assess the entomological risk related to human exposure to dengue regarding the abundance and distribution pattern of Ae. aegypti and Ae. albopictus in Kinshasa, the Democratic Republic of the Congo.

4. DiscussionThe overall results from the present study reveal that Aedes mosquitoes are most abundant during the rainy season. Most larvae habitats are anthropogenic due to the management of water stocking, and the mismanagement of environmental and ecological factors are among the drivers of mosquito occurrence. In suburban municipalities which lack permanent water supply sufficient for domestic uses, most larvae habitats are the domestic containers used to stock water. In most resident plots from these municipalities, people set a outdoor big water container or multiple small containers to collect the rainwater; this observation might explain, in part, the abundance of mosquitoes during the rainy season in these areas. Even in the dry season, the outdoor containers are used to stock water, but some of them remain uncovered. This observation is more documented in the areas with small house sizes, likely due to limited space indoors, and in places where construction activities are undertaken, as most people prefer to build during the dry season. Inadequate and irregular water supplies are known as driving factors of mosquito abundance in many locations [37,38]. Although discarded containers are found everywhere in Kinshasa, they were predominant in most populated areas, as well as the advanced urbanization or uncontrolled urbanization areas such as Matete, Kasa-Vubu, Barumbu, Limete, and Kinshasa. The tires were a larvae habitat widely distributed over the whole of Kinshasa, but mostly in the municipalities where automobiles garage activities or related activities were practiced such as in Ndjili, Kasa-Vubu, Ngiri-Ngiri, and Ngaliema (Delvaux), and in municipalities with relatively high socioeconomic status such as Lingwala, Limete, Kasa-Vubu, Masina (sans fil), Barumbu, and Bandalungwa, likely because people from rich municipalities can afford a vehicle or car and can change damaged tires and keep them outside their homes. In addition, the tire trade is common in those areas. The findings from the studies in Pakistan and Iran underline the roles of the tire trade in spreading dengue vectors in new areas previously not known endemic to dengue [39,40]. The bamboos were larvae habitats mainly in municipalities that lay on or crossed by water bodies and in highland areas.These municipalities face soil erosion, and bamboo is planted to stabilize the soil and control the erosion. However, bamboo is known to be one of the most productive larvae habitats due to its water salinity and dissolved oxygen [24]. In addition, some people have created large ground pits to retain rainwater to prevent landslides in their neighborhoods. Such practice is contributing to increasing mosquito production in these areas. Both Aedes species are widely distributed in Kinshasa, but not homogeneously. Aedes albopictus is slightly predominant in suburban areas, likely due to the high level of vegetation coverage. This observation is inconsistent with the findings from the literature [41,42].Dengue contributes to the burden of febrile illness in Kinshasa. However, due to lack of attention that it has received by medical practitioners and the lack of appropriate diagnostic tools in most areas of sub-Saharan African countries, it remains underdiagnosed [43]. Findings from different studies have reported that NS1 RDTs have high specificity; their sensitivity can be affected by the time of sampling and dengue serotypes [44,45]. However, this performance of RDT in the acute phase of dengue is enhanced once it is combined NS1 with IgM/IgG RDT [46]. Indeed, the use of these combined types of RDTs provides an advantage to the study participants regarding information about chronic and active infections. IgM is produced early during the acute phase of the disease and disappears very soon. However, IgG is produced later and can remain longer; therefore, it can reveal a past exposure [1]. The current serosurvey was carried out during the dry season, and the presence of the dengue IgG was recorded in 38 participants. High-level exposition to dengue may occur more frequently during the rainy season, as Ae. aegypti and Ae. albopictus are abundant during that period. Detection of the IgM antibody and NS1 among participants highlights the importance to consider dengue as the major etiology of febrile illness in Kinshasa, where only 29.0% of participants had positive results of malaria RDT and 2.0% were coinfected by both microorganisms. Similar results were reported in Kinshasa in 2018, in a hospital-based survey, with an acute dengue frequency of 8.1% using dengue RDT and ELISA. Among 19 cases of acute dengue, 36.1% were positive to malaria; however, the frequency appeared slightly higher than the 24.2% reported in the current study among presented acute dengue fever [21].In our study, in two households from different locations (the Kinshasa and Limete (Kingabwa) municipalities), the IgM and NS1 antigen were detected in two members of the same household, and both members presented similar clinical manifestations. This observation confirmed that human is the reservoir of this virus in an urban area, and the infection is actively transmitted between humans through infected mosquito bites in places where the competent vector exists [1]. In the Kinshasa municipality as well as in its neighboring municipalities (Lingwala, Barumbu) from Lukunga, Ae. aegypti was the predominant species. In 2022, cases of yellow fever outbreak were recorded in Kinshasa, Kimbanseke, precisely in the Kingasani health zones and Mont Ngafula municipalities [30]. The high demographical density with increasing population movement is known, among other factors, to spread infection to other areas. This observation is supported by the observation made during the wide yellow fever epidemic that occurred in Angola and the DRC in 2016 [47]. Similar to the geographical distribution of Aedes, the magnitude of human exposure varied also according to district and within the district from one municipality to another.Considering the Tshangu district, of the blood samples tested in the Ndjili municipality, only one case was recorded using an NS1 RDT. However, this municipality was classified among those at high entomological risk of MBVD regarding the number of Aedes-positive container index and grid cells (44%). It is important to also the genetic population diversity and their competence to transmit different MBVDs. The competence varies according to the genetic population, which can also vary according to geographical location [48]. The Mont Amba district had a high number of seropositive cases. However, both Aedes species were recorded approximately at the same rate: Ae. albopictus slightly predominated in Kisenso. Matete (Maziba namely also De Marrais) and Limete (Kingabwa, Ndanu, Salongo, and Mombele areas), which are humid areas laid on the Ndjili and Congo Rivers, favorable conditions for mosquito multiplication. Early wide chikungunya outbreaks in 1999–2000 have occurred in Kingabwa, De Marrais, and Kikole in Nsele [49]. In these areas, Aedes should maintain their activity even during the dry season; this argument might explain the occurrence of active cases (NS1-, IgM-positive) recorded in the dry season. In the Funa district, in general, Ae. aegypti was predominant. Only IgG antibodies were detected among participants from the municipalities of Selembao and Bumbu, while cases of acute dengue were noted in the Kokolo military camp. However, the entomological baseline data was missed in the Bumbu municipality; during the inspection of the home place of the positive cases, we noted that automobile garage activities were widely undertaken in this municipality, leading to a high presence of discarded tires that should be the important source of mosquitoes. In Lukunga, the Aedes species’ composition varied according to the municipality. The Ae. eagypti and Ae. albopictus were recorded at approximately the same rate in Ngaliema, and Ae. albopictus slightly predominated where vegetation coverage appeared relatively high in Mont Ngafula and Ngaliema. The seropositivity was recorded as follows: The two positive cases from Gombe were recorded in a military camp built closer to the Congo River; this highly populated area is surrounded by many boat beaches, which connect Kinshasa with other provinces known at high risk of MBVD such as yellow fever [19]. The young age, the male sex, and the residence location adjusted to the participant’s marital status, occupation, and education level appeared as risk factors for dengue exposure occurrence.These findings describe the population stratus that might be the priority for targeting control activities. Often, males are involved in professions that can expose them to increased mosquito bites such as those working in forested areas, automobiles mechanics, and military camps. Overall, four cases of acute dengue were recorded in both military camps involved in the current study. The militaries are among the social categories with an increasing trend of migration; in 1998, an outbreak of arboviruses occurred in a military camp in the province of Tshopo located in the northeastern part of the DRC [50]. The evidence of a higher prevalence of arboviruses among males has been documented in the literature [51]. The findings of this study also call for social mobilization, education programs to encourage the population to actively and persistently participate in the cleanliness of their living environment as it is within their reach, and adoption of protective behaviors against mosquito bites.Despite the relevant findings reported in the current study, this study aimed solely aimed to gain insight into human exposure to dengue. This study had some limitations. The Flavivirus is known to present the cross-reactivity of IgG antibodies among these viruses’ family members [52], and the test specificity can be affected. The tests also detected IgM, and it has been coupled with the NS1 RDT, known as a more specific and sensitive marker for the primary cases of dengue. Therefore, the performance of our diagnostic maintained good consistency with available data from the literature [21,42,43,46]. Mostly due to a lack of study sufficient funds and time constraints, the performance of our diagnostic method was not compared to the standard diagnostic methods for the serology, such as enzyme-linked immunosorbent assays (ELISA) and the molecular detection of NS1 by RT-PCR. In addition, the number of participants tested was unequal among municipalities, with fewer participants in some municipalities. To facilitate the inclusion of the study and the blood sampling, the hospital-based survey and study design were used and allowed to include only febrile patients who attended the healthcare facilities. A community-based survey with a large sample size could provide more information related to the extent of human exposure.

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