ORIGINAL RESEARCH article
Sec. Vector Biology
Physicochemical Characteristics of Aedes Mosquito Breeding Habitats in Suburban and Urban Areas of Kinshasa, Democratic Republic of the Congo
- 1SACIDS Africa Centre of Excellence for Infectious Diseases of Humans and Animals in Eastern and Southern Africa, Sokoine University of Agriculture, Morogoro, Tanzania
- 2Department of Tropical Medicine, Infectious and Parasitic Diseases, University of Kinshasa, Kinshasa, Democratic Republic of Congo
- 3Department of Veterinary Microbiology, Parasitology and Biotechnology, Sokoine University of Agriculture, Morogoro, Tanzania
- 4Department of Veterinary Medicine and Public Health, Sokoine University of Agriculture, Morogoro, Tanzania
Background: The knowledge of key elements of the ecosystem affecting mosquito distribution and their population dynamics is essential for designing mosquito-borne disease interventions. The present study characterized the physicochemical properties of Aedes mosquito breeding habitats in Democratic Republic of the Congo.
Methods: A cross-sectional survey was carried out in Kinshasa, from February to April 2021. The physicochemical characteristics of the natural and artificial aquatic habitats of Aedes were measured using a multiparametric device.
Results: Out of 438 breeding habitats inspected, 273 (62.3%) contained mosquito larvae. The Aedes mosquitoes identified in 76.19% of positive breeding sites were Aedes albopictus (67.30%) and Aedes aegypti (37.98%). The median values of dissolved oxygen (DO) (1.0), turbidity (19.15), and salinity (0.115) in water breeding sites of Aedes were respectively 0.8, 55.0, and 0.29 in Culex breeding sites (p < 0.05). The physicochemical characteristics of the breeding habitat for Ae. aegypti and Ae. albopictus were almost identical. In urban areas, the median temperature was 29.82 while it was 29.60 in suburban areas (p < 0.05). Significantly, the salinity was higher in bamboo and metal containers while DO was higher in tins. After analysis using simple linear regression, total dissolved solids (r = 0.23; p = 0.000), conductivity (r = 0.23), salinity (r = 0.23), and temperature (r = 0.13) were associated with larval density (p < 0.05). In the final model (r = 0.30, p = 0.01), salinity (r = 0.23) and DO (r = 0.138) adjusted to temperature, pH, and turbidity were associated positively to larvae density.
Conclusion: The Aedes breeding sites and mosquito density were significantly influenced by water salinity, DO, temperature, pH, and turbidity.
Chikungunya, Zika, yellow fever, and dengue have reemerged and emerged as an important public health challenge worldwide as well in the Democratic Republic of the Congo (DRC) (1–3). These mosquito-borne viral diseases (MBVD) are mainly transmitted by Aedes mosquitoes. Aedes aegypti and Ae. albopictus are known to be the major vectors of most of the MBVD (4, 5). Multiple factors ranging from climatic, environmental, ecological, and socioeconomic factors exert influence over arbovirus vectors distribution and abundance (6, 7).
Mosquito immature stages are entirely aquatic and require water for their development. Various water-holding containers ranging from small to large and natural to manmade have been reported to support Aedes mosquito breeding. They include tires, flower pots, plastic or metal recipients, drains, swimming pools, storm water, flooding water, bamboo sticks, and plant axils (8–10). Moreover, any standing water body represents a potential mosquito breeding site. The quality of the water might selectively favor the development of larvae and pupae of some mosquitoes species and successful development into adult mosquitoes (11. The choice of breeding sites by mosquitoes is a key element for mosquito productivity, population survival, and dynamics (12).
The physicochemical characteristics of a mosquito breeding site express a significant influence on the immature stage of the mosquito life cycle and have important implications for mosquito control (9, 13). Some of these characteristics such as pH, salinity, dissolved oxygen (DO), and total dissolved solids (TDS) have been shown to influence the density of Ae. aegypti and Ae. albopictus (14, 15). These water characteristics affect some mosquito basic features such as survival, body size, and biting behavior which are linked to mosquito vectorial capacity, hence the magnitude and intensity of disease transmission. Indeed, the deficit of food supply in the stage of immature mosquito development leads to hatching of small mosquito adult body size and decrease in longevity (16). Habitually, the small female mosquitoes are more active in host seeking and blood feeding than the larger-size females probably due to limited energy stock to support egg maturation (17). Therefore, this behavior modification exposes hosts to high mosquito biting rates with possibility of pathogen transmission (17, 18). Thus, water availability and storage procedures greatly influence mosquito immature richness and MBVD risk occurrence (19).
The majority of large cities of DRC including Kinshasa are characterized by heterogeneous levels of urbanization and unequal levels of pollution. With the geographical expansion of chikungunya and dengue and repeated yellow fever outbreaks in DRC, there is a need to improve our understanding of the vector ecological factors (20–22). The physicochemical and environmental factors in mosquito breeding sites exert an effect on the density of mosquito larvae as well as on their detoxification enzyme activities. They can present an impact on insecticide resistance occurrence (23). It has been reported that the management of the pH of favored breeding sites could serve as a tool to control mosquito, and it can also assist the choice of biopesticides to use (24). Therefore, the good knowledge on Aedes breeding site physicochemical properties is critical in the design of effective vector interventions (25).
Not much data are currently available on the physicochemical characteristics of Aedes mosquito larval habitats in DRC. The present study assessed the physicochemical characteristics of Aedes water breeding habitats in the urban and suburban areas of Kinshasa, DRC.
Study Area and Selection of Study Sampling Sites
The study was carried out in Kinshasa, situated in the western part of DRC at latitudes 4°19′30′S and longitudes 15°19′20′E. Kinshasa is the capital province of DRC and the largest metropolis in Central Africa with a population of 12 million inhabitants. Kinshasa occupies an area of 9,965 km2, of which only 10% represents urban areas. Kinshasa receives over 1,482 mm of rainfall annually with average temperature of 25.2°C. There are two marked seasons, a rainy season from October to the first half of May and a dry season from the second half of May to September. The topography consists of larger plains surrounded by some hills, with a significant hydrographic system. The soils are sandy and sandy-argillaceous. Kinshasa is divided into 24 municipalities (26, 27).
The study sampling sites (Figure 1) were chosen to reflect the wide range of different conditions within the region in terms of urbanization level, environmental parameters that are likely to promote active transmission of arboviral infections, proximity to rivers, and a history of occurrence of arboviral disease outbreaks (5, 21, 28, 29).
Study Design and Mosquito Collection
This cross-sectional survey was carried out from February to April 2021. At all study sites, various natural and artificial containers were inspected for the presence of immature stages of mosquitoes. The larval densities of each immature mosquito breeding habitats were determined.
Depending on the mosquito habitat size, larvae and pupae were collected by either dipping or pipetting or emptying the container. Water samples were collected in 350-ml plastic containers. All mosquito larvae and pupae for each habitat were counted to determine the density. The collected larvae and pupae were reared into adult. Rearing was done under ambient temperature 28°C and relative humidity 80% with a 12:12-h (light: dark) photoperiod. All hatched adult mosquitoes were identified into genera using morphological identification keys. Afterward, a pictorial key was used to identify Aedes mosquito into species (30).
Physicochemical Parameter Measurement
Water samples from each inspected container were collected and analyzed for the following physicochemical parameters: pH, temperature, TDS (mg/l), DO (%), salinity (practical salinity unit), turbidity (Formazin Nephelometric Unit), and conductivity (μS/cm)using an electronic device (HANNA© HI9829). This device was regularly calibrated as per owners’ manual.
The data were entered into the Microsoft Excel 2007 spreadsheet and analyzed using GraphPad Prism version 9.1.2 for Windows (GraphPad Software, San Diego, CA, USA). Descriptive statistics were applied to summarize data. Due to non-normality of data distribution based on the Shapiro–Wilk test, the differences of the physicochemical characteristics in Aedes, Anopheles, Culex, and negative breeding habitats and between different Aedes habitats types were tested using the Kruskal–Wallis test with Dunn’s multiple-comparison test as post-hoc test. The Mann–Whitney U test was used to compare the medians of the physicochemical characteristics between urban and suburban areas and between Ae. aegypti and Ae. albopictus breeding sites. The simple and multiple-regression linear analyses were applied to investigate the relationship between mosquito larval densities and the physicochemical factors of the breeding water. For all the statistical analysis, p value < 0.05 was considered significant.
A total of 438 water-breeding places were inspected. Of these, 273 contained mosquito larvae including 90 (32. 97%) tires, 56 (20.51%) plastic containers, 43 (15.82%) collections of stagnant and flooding water, 17 (6.23%) bamboo sticks, 16 (5.86%) tins, and 14 (5.13%) metal containers (Table 1). Aedes spp. were found in 208 (76.19%) breeding sites; 79 (28.94%) breeding sites were positive for Culex spp.; 21 (7.69%) had Anopheles spp.; and three (1.09%) had Toxorhynchites mosquitoes. The co-occurrence of Aedes spp. and Culex spp. was recorded in 23 (8.42%) breeding sites, while in seven (2.56%) breeding sites, Aedes cohabited with Anopheles. Of 208 positive Aedes spp. habitats, Ae. albopictus were found in 140 (67.30%) sites and Ae. aegypti in 79 (37.98%) sites, while in 23 breeding habitats, the two species of Aedes were found together (Table 2).
Table 2 Frequency of breeding sites of mosquito species occurrence and co-occurrence recorded in Kinshasa.
The overall trends of physicochemical characteristics of the positive breeding habitats were significantly different from the ones without mosquito larvae (Table 3). Using Dunn’s multiple-comparison test as post-hoc test, the median of DO was significantly higher in water breeding sites of Aedes (1.0) compared to Culex mosquitoes (0.8), p = 0.0001. Respectively, the means of conductivity (228.5), TDS (112.5), turbidity (19.5), and salinity (0.115) in water breeding sites of Aedes were significantly lower than in Culex (555.0, 267.0, 55.0, and 0.29) with p < 0.05. The pH in the Aedes breeding site (6.76) was higher than in Anopheles (6.58) with p = 0.0002. The patterns of physicochemical characteristics favoring different mosquito occurrence are summarized in Figure 2.
Table 3 Comparison of the medians of the physicochemical characteristics of water from positive and negative larvae habitats of mosquito in Kinshasa.
Figure 2 Comparison of physicochemical characteristics of breeding habitats between Aedes, Culex, and Anopheles mosquito in Kinshasa. (A) pH, (B) dissolved oxygen, (C) conductivity, (D) total dissolved solids, (E) salinity, (F) turbidity, (G) temperature. *P < 0.05, **P ≤ 0.01, ***P ≤ 0.001, ****P ≤ 0.0001 and ns, not significant (P > 0.05).
The percentage of DO in Aedes breeding habitats ranged from 0.5 to 2.6. The medians of DO, pH, conductivity, salinity, TDS, and turbidity as well as temperature of Aedes breeding habitats are provided in Table 4. Ae. aegypti and Ae. albopictus were found breeding in water sites with related properties as regards turbidity, salinity, pH, TDS, DO, conductivity, and temperature levels (Table 5). Compared to suburban areas, the median of conductivity in urban areas was 236 vs. 228, U = 5088, p = 0.7118; TDS (109.5 vs. 114.5, U = 5141, p = 0.8059) and salinity (0.12 vs. 0.115, U = 5084, p = 0.7046). The median of temperature was significantly high in urban areas (29.82) than in suburban areas 29.60, U = 4319, p = 0.0298 (Table 6). Some of these physicochemical parameters varied significantly according to the larval habitat types. A high percentage of DO was recorded in tin (1.2) and tire (1.05) and lower % DO in stagnant water (0.7) and sewage pit (0.65); U p = 0.0014. The salinity was high in bamboo sticks (0.31) and lower in tin (0.04), p = 0.0001. The trends of different physicochemical parameters of the different breeding Aedes habitats are summarized in Table 7.
Table 5 Comparison of the medians of physicochemical characteristics favoring Ae. aegypti and Ae. albopictus occurrence using the Mann–Whitney test.
Table 6 Comparison of the medians of physicochemical characteristics of Aedes spp. breeding sites according to urbanization level.
Table 7 Comparison of the medians of the physicochemical parameters according the type of breeding habitat of Aedes in Kinshasa.
In simple linear regression, the larval density in Aedes breeding habitats showed a positive relationship with TDS (r(206) = 0.23; p = 0.001), conductivity (r(206) = 0.23; p = 0.001), salinity (r(206) = 0.23; p = 0.001), and temperature (r(206) = 0.138; p = 0.04) (Table 8). In the multiple linear regression model (r(202) = 0.30, p = 0.002), salinity (r = 0.23, p = 0.001) and DO = 0.138, p = 0.047) adjusted to temperature, pH, and turbidity were positively associated with larval density (Table 9).
Table 8 Simple linear regression analysis of breeding habitat characteristics in relation to the larvae density into Aedes breeding habitats in Kinshasa.
Table 9 Multiple regression analysis model of breeding habitat characteristics in relation to the larval density into Aedes breeding habitats in Kinshasa.
The present study addressed the association between physicochemical properties of Aedes mosquito habitats in urban and suburban areas of Kinshasa. Infestation with Ae. albopictus and Ae. aegypti accounted for the over three-quarters of the breeding sites. Ae. aegypti and Ae. albopictus bred in water sites with closely related turbidity, pH, TDS, DO, conductivity, and temperature levels. However, these Aedes species preferred less turbid waters with moderate salinity and moderate DO. The findings of this study revealed differences in some parameters such as TDS, DO, conductivity, turbidity, and salinity according to the level of urbanization and habitant types, either natural or artificial. This is contrary to the findings from Zanzibar in Tanzania where the presence of immature Ae. aegypti was not linked significantly to any physicochemical characteristics of water breeding habitats (31).
Indeed, Kinshasa is characterized by uncontrolled and heterogeneous urbanization levels, poor environmental hygiene, multiple soil erosion, and recently multiple floodings (26, 27, 32). These conditions create suitable mosquito breeding habitats. The quality of water within these habitats varies in terms of their physicochemical characteristics which can promote or limit the proliferation of some Aedes species. The physicochemical parameters of Ae. aegypti and Ae. albopictus breeding site water were similar in regard to turbidity, pH, salinity, chloride, and phosphate levels (24).
Similar to findings from other studies, containers expressed differences in water physicochemical profile and urbanization considerably accelerates the larval development rate and survival time of adult of Ae. albopictus, with a positive effect on vector capacity (17). The anthropogenic Ae. aegypti prefers clean water found in various types of peridomestic containers while Ae. albopictus prefers natural containers or outdoor manmade habitats containing abundant amounts of organic debris (19). The temperature, DO, and pH of breeding site water have differences between endemic and non-endemic areas (33). The physicochemical and biological markers of mosquito larval habitats help in mapping of areas suitable for breeding and distribution for targeting surveillance and controlling activities (17, 34).
Reports from different environments show a relationship between physicochemical characteristics of immature habitats and container types. However, differences in some parameters could be linked to the nature of the container, either natural or artificial, and water source (19, 35, 36). In the current study, various natural and artificial breeding habitats of immature mosquitoes were explored and grouped according to their materials made. They exhibited a significant difference in their physicochemical properties. The concentration of TDS and the levels of turbidity and conductivity were low in tin and plastic container. The non-household locations, as well as non-disposable containers, should be targeted in the standard control activities of mosquito-borne viral diseases (37), contrary to findings from Tanzania where the presence of immature Ae. aegypti was not linked significantly to any physicochemical characteristics of water breeding habitats (31). In other studies, it was reported that the selection of breeding sites depends on the volume and size of the water surface and the type of material of which they are made (38.). Aedes mosquito prefers materials which are made from cement, metal, soil, ceramics, and plastic (36, 39.). In a study in Kolkata, India, plastic containers were reported as the most productive habitats for Aedes species (35). The populations of immature mosquitoes growing in ground pools are exposed to diverse factors of death, natural enemies compared to those in water-filled containers in which the growth is restricted by food availability (38).
Although in simple linear regression, larval density showed a positive relationship with the temperature, concentration of TDS, conductivity, and salinity, in multiple linear regression analysis, only salinity and DO adjusted to temperature, pH, and turbidity were associated with increasing larval density. This observation was in agreement with findings from a study in Egypt (40). It was also reported from Iran that DO presents a significant impact on larval density (41). The salinity is another parameter that can promote or limit the growth of larvae (40–43). Temperature affects the degree of evapotranspiration, and therefore, it acts on the water salinity (43). Water temperature is a crucial parameter for mosquito metabolism and development (17, 38, 44). In other studies, the breeding site characteristics of Ae. albopictus showed a negative correlation of the larval density with turbidity and conductivity but a positive correlation with pH and DO (40, 42, 43, 45). Water pH and turbidity in the current study seemed to decrease larval density, but the association was not significant. Similar findings have been reported from a study in Iran (44).
Most of Ae. aegypti and Ae. albopictus aquatic breeding habitats are temporary, disappearing during the dry season. Therefore, it was difficult to repeat the measurement of these physicochemical parameters in the same surveyed water habitats to assess the effect of seasonality on the physicochemical characteristics of Aedes. Considering that the physicochemical parameters were measured only once in this study and during the raining season, it is aware to consider the probability of larval habitat physicochemical characteristics and larval density fluctuation due to seasonality. Furthermore, studies are essential to consider not only the effect of the abiotic factors (the physicochemical characteristics) on larval productivity in breeding sites but also the effect that can express the biotic factors such as larval predators, algae, and emergent plants on larval productivity in Aedes breeding habitats in order to consolidate the baseline information on mosquito larval habitat characteristics.
The current study showed that the salinity and percentage of DO exert influence on the distribution of Aedes mosquito occurrence, survival, and abundance. Other parameters such temperature, acidity or alkalinity, and turbidity indirectly influence Aedes mosquito proliferation. Environment factors such urbanization and the nature of breeding habitat affect these physicochemical parameters. The findings of this study can assist in designing control activities of Aedes-borne diseases by targeting areas suitable for breeding.
Data Availability Statement
The original contributions presented in the study are included in the article/Supplementary Material. Further inquiries can be directed to the corresponding author.
KM designed the study, conducted the fieldwork, performed the statistical analysis, and prepared the manuscript for publication. RW, PM, and SIK assisted in the study design. DE, MB, and JZ participated in the fieldwork. LM and GM critically read the manuscript for publication. All authors contributed to the article and approved the submitted version.
KM is a recipient of a PhD scholarship from the Government of the United Republic of Tanzania through the World Bank (WB-ACE II Grant PAD1436, IDA credit 5799-TZ) to the SACIDS Africa Centre of Excellence for Infectious Diseases at the Sokoine University of Agriculture.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
The authors thank the Department of Tropical Medicine, Infectious and Parasitic Diseases of University of Kinshasa for materials assistance during the field works.
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fitd.2021.789273/full#supplementary-material
Additional File 1 | Dataset supporting the conclusions of study on physico-chemicals characteristics of Aedes breeding sites in Kinshasa.
MBVD, mosquito-borne viral disease; DO, dissolved oxygen; TDS, total dissolved solid; DRC, Democratic Republic of the Congo.
1. Li Z, Wang J, Cheng X, Hu H, Guo C, Huang J, et al. The Worldwide Seroprevalence of DENV, CHIKV and ZIKV Infection: A Systematic Review and Meta-Analysis. PLoS Negl Trop Dis (2021) 15:e0009337. doi: 10.1371/journal.pntd.0009337
2. Mbanzulu KM, Mboera LEG, Luzolo FK, Wumba R, Misinzo G, Kimera SI. Mosquito-Borne Viral Diseases in the Democratic Republic of the Congo: A Review. Parasit Vectors (2020) 13:103. doi: 10.1186/s13071-020-3985-7
4. Luza AL, Gualdi CB, Diefenbach LML, de AG, Schüler-Faccini L, Ferraz G. Dynamic Mapping of the Probability of Infestation by Urban Arbovirus Vectors in the Municipalities of Rio Grande do Sul State, Brazil 2016-2017. Epidemiol Serv Saúde (2021) 30:e2020154. doi: 10.1590/s1679-49742021000200006
5. Wat’senga Tezzo F, Fasine S, Manzambi Zola E, Marquetti M, del C, Binene Mbuka G, et al. High Aedes Spp. Larval Indices in Kinshasa, Democratic Republic of Congo. Parasit Vectors (2021) 14:92. doi: 10.1186/s13071-021-04588-7
6. Adnan RA, Ramli MF, Othman HF, Asha’ri ZH, Ismail SNS, Samsudin S. The Impact of Sociological and Environmental Factors for Dengue Infection in Kuala Lumpur, Malaysia. Acta Trop (2021) 216:105834. doi: 10.1016/j.actatropica.2021.105834
7. Morgan J, Strode C, Salcedo-Sora JE. Climatic and Socio-Economic Factors Supporting the Co-Circulation of Dengue, Zika and Chikungunya in Three Different Ecosystems in Colombia. PLoS Negl Trop Dis (2021) 15:e0009259. doi: 10.1371/journal.pntd.0009259
8. Dida GO, Anyona DN, Abuom PO, Akoko D, Adoka SO, Matano A-S, et al. Spatial Distribution and Habitat Characterization of Mosquito Species During the Dry Season Along the Mara River and Its Tributaries, in Kenya and Tanzania. Infect Dis Poverty (2018) 7:2. doi: 10.1186/s40249-017-0385-0
9. Gao Q, Wang F, Lv X, Cao H, Su F, Zhou J, et al. Aedes Albopictus Production in Urban Stormwater Catch Basins and Manhole Chambers of Downtown Shanghai, China. PLoS One (2018) 13:e0201607. doi: 10.1371/journal.pone.0201607
11. Medeiros-Sousa AR, Oliveira-Christe R, Camargo AA, Scinachi CA, Milani GM, Urbinatti PR. Influence of Water’s Physical and Chemical Parameters on Mosquito (Diptera: Culicidae) Assemblages in Larval Habitats in Urban Parks of São Paulo, Brazil. Acta Trop (2020) 205:105394. doi: 10.1016/j.actatropica.2020.105394
12. Sultana A, Hasan S, Hossain M, Alim A, Mamun MA, Bashar K. Larval Breeding Habitats and Ecological Factors Influence the Species Composition of Mosquito (Diptera : Culicidae) in the Parks of Dhaka City, Bangladesh. Bangladesh J Zool (2017) 45:111–22. doi: 10.3329/bjz.v45i2.35706
13. Selvan PS, Jebanesan A, Divya G, Ramesh V. Diversity of Mosquitoes and Larval Breeding Preference Based on Physico-Chemical Parameters in Western Ghats, Tamilnadu, India 2015. Asian Pac J Trop Dis (2015) 5:S59–66. doi: 10.1016/S2222-1808(15)60858-1
15. Nikookar SH, Fazeli-Dinan M, Azari-Hamidian S, Mousavinasab SN, Aarabi M, Ziapour SP, et al. Correlation Between Mosquito Larval Density and Their Habitat Physicochemical Characteristics in Mazandaran Province, Northern Iran. PLoS Negl Trop Dis (2017) 11:e0005835. doi: 10.1371/journal.pntd.0005835
16. Jeffrey Gutiérrez EH, Walker KR, Ernst KC, Riehle MA, Davidowitz G. Size as a Proxy for Survival in Aedes Aegypti (Diptera: Culicidae) Mosquitoes. J Med Entomol (2020) 57:1228–38. doi: 10.1093/jme/tjaa055
17. David MR, Dantas ES, Maciel-de-Freitas R, Codeço CT, Prast AE, Lourenço-de-Oliveira R. Influence of Larval Habitat Environmental Characteristics on Culicidae Immature Abundance and Body Size of Adult Aedes Aegypti. Front Ecol Evol (2021) 9:626757. doi: 10.3389/fevo.2021.626757
18. Bara J, Rapti Z, Cáceres CE, Muturi EJ. Effect of Larval Competition on Extrinsic Incubation Period and Vectorial Capacity of Aedes Albopictus for Dengue Virus. PLoS One (2015) 10:e0126703. doi: 10.1371/journal.pone.0126703
19. Overgaard HJ, Olano VA, Jaramillo JF, Matiz MI, Sarmiento D, Stenström TA, et al. A Cross-Sectional Survey of Aedes Aegypti Immature Abundance in Urban and Rural Household Containers in Central Colombia. Parasit Vectors (2017) 10:356. doi: 10.1186/s13071-017-2295-1
20. Otshudiema JO, Ndakala NG, Mawanda EK, Tshapenda GP, Kimfuta JM, Nsibu L-RN, et al. Yellow Fever Outbreak — Kongo Central Province, Democratic Republic of the Congo, August 2016. MMWR Morb Mortal Wkly Rep (2017) 66:335–8. doi: 10.15585/mmwr.mm6612a5
21. Selhorst P, Makiala-Mandanda S, Smet BD, Mariën J, Anthony C, Binene-Mbuka G, et al. Molecular Characterization of Chikungunya Virus During the 2019 Outbreak in the Democratic Republic of the Congo. Emerg Microbes Infect (2020) 9:1912–8. doi: 10.1080/22221751.2020.1810135
22. Willcox AC, Collins MH, Jadi R, Keeler C, Parr JB, Mumba D, et al. Seroepidemiology of Dengue, Zika, and Yellow Fever Viruses Among Children in the Democratic Republic of the Congo. Am J Trop Med Hygiene (2018) 99:756–63. doi: 10.4269/ajtmh.18-0156
23. Imam AA, Deeni Y. Larval Productivity and Detoxification Enzymes Profile in Response to Physico-Chemical Environmental Factors of Anopheles Gambiae Breeding Ecologies in Nigeria. Curr J Appl Sci Technol (2015) 5:595–612. doi: 10.9734/BJAST/2015/13268
25. Liang G, Gao X, Gould EA. Factors Responsible for the Emergence of Arboviruses; Strategies, Challenges and Limitations for Their Control. Emerg Microbes Infect (2015) 4:1–5. doi: 10.1038/emi.2015.18
26. Mvemba NNNJ, Aloni KJ, Binzangi KL, Lapika DB, Paulus JJ, Nkodila NA, et al. Causes and Consequences of the Destruction of Green Spaces in the City of Kinshasa, the Democratic Republic of Congo. Int J Health Sci Res (2021) 11:84–9.
27. World Bank. Revue De L’urbanisation En République Démocratique Du Congo: Des Villes Productives Et Inclusives Pour L’émergence De La République Démocratique Du Congo. Directions in Development—Environment and Sustainable Development. Washington, DC: World Bank (2018). Available at: https://openknowledge.worldbank.org/handle/10986/28931 (Accessed 5 June 2021).
28. Mbanzulu KM, Wumba R, Mukendi J-PK, Zanga JK, Shija F, Bobanga TL, et al. Mosquito-Borne Viruses Circulating in Kinshasa, Democratic Republic of the Congo. Int J Infect Dis (2017) 57:32–7. doi: 10.1016/j.ijid.2017.01.016
29. Muyembe-Tamfum JJ, Peyrefitte CN, Yogolelo R, Mathina Basisya E, Koyange D, Pukuta E, et al. Epidemic of Chikungunya Virus in 1999 and 200 in the Democratic Republic of the Congo. Med Trop (Mars) (2003) 63:637–8.
31. Saleh F, Kitau J, Konradsen F, Alifrangis M, Lin C-H, Juma S, et al. Habitat Characteristics For Immature Stages of Aedes Aegypti In Zanzibar City, Tanzania. J Am Mosquito Control Assoc (2018) 34:190–200. doi: 10.2987/17-6709.1
32. Bédécarrats F, Lafuente-Sampietro O, Leménager M, Lukono Sowa D. Building Commons to Cope With Chaotic Urbanization? Performance and Sustainability of Decentralized Water Services in the Outskirts of Kinshasa. J Hydrol (2019) 573:1096–108. doi: 10.1016/j.jhydrol.2016.07.023
33. Hidayah N, Rahmawati D. Bio-Physicochemical Markers of the Aedes Aegypti Breeding Water in Endemic and Non-Endemic Area. Int J Public Health Sci (IJPHS) (2019) 8:151. doi: 10.11591/ijphs.v8i2.18883
34. Amini M, Hanafi-Bojd AA, Aghapour AA, Chavshin AR. Larval Habitats and Species Diversity of Mosquitoes (Diptera: Culicidae) in West Azerbaijan Province, Northwestern Iran. BMC Ecol (2020) 20:60. doi: 10.1186/s12898-020-00328-0
35. Chatterjee S, Chakraborty A, Sinha SK. Spatial Distribution & Physicochemical Characterization of the Breeding Habitats of Aedes Aegypti in & Around Kolkata, West Bengal, India. Indian J Med Res (2015) 142:S79–86. doi: 10.4103/0971-5916.176631
37. Troyo A, Calderón-Arguedas O, Fuller DO, Solano ME, Avendaño A, Arheart KL, et al. Seasonal Profiles of Aedes Aegypti (Diptera: Culicidae) Larval Habitats in an Urban Area of Costa Rica With a History of Mosquito Control. J Vector Ecol (2008) 33:76. doi: 10.3376/1081-1710(2008)33[76:SPOAAD]2.0.CO;2
39. Mboera LEG, Mweya CN, Rumisha SF, Tungu PK, Stanley G, Makange MR, et al. The Risk of Dengue Virus Transmission in Dar Es Salaam, Tanzania During an Epidemic Period of 2014. PLoS Negl Trop Dis (2016) 10:e0004313. doi: 10.1371/journal.pntd.0004313
40. Kenawy MA, Ammar SE, Abdel-Rahman HA. Physico-Chemical Characteristics of the Mosquito Breeding Water in Two Urban Areas of Cairo Governorate, Egypt. J Entomol Acarol Res (2013) 45:e17. doi: 10.4081/jear.2013.e17
41. Oniya M, Akintayo A, Olusi T. Ecological Factors Favouring Mosquito Breeding in Ifedore Local Government Area of Ondo State, Nigeria. J Ecol Natural Environ (2019) 11:68–74. doi: 10.5897/JENE2019.0756
42. Emidi B, Kisinza WN, Mmbando BP, Malima R, Mosha FW. Effect of Physicochemical Parameters on Anopheles and Culex Mosquito Larvae Abundance in Different Breeding Sites in a Rural Setting of Muheza, Tanzania. Parasit Vectors (2017) 10:304. doi: 10.1186/s13071-017-2238-x
43. Gopalakrishnan R, Das M, Baruah I, Veer V, Dutta P. Physicochemical Characteristics of Habitats in Relation to the Density of Container-Breeding Mosquitoes in Asom, India. J Vector Borne Dis (2013) 50:215–9.
44. Omrani S-M, Azari-Hamidian S. Vertical Distribution, Biodiversity, and Some Selective Aspects of the Physicochemical Characteristics of the Larval Habitats of Mosquitoes (Diptera: Culicidae) in Chaharmahal and Bakhtiari Province, Iran. Int J Epidemiol Res (2020) 7:74–91. doi: 10.34172/ijer.2020.15
45. Messai N, Aouati A, Berchi S. Impact of the Surface Water Physicochemical Parameters on Culicidae (Diptera: Nematocera) of Lakeside Ecosystem “Sebkhet Ezzemoul” (Oum El Bouaghi -Algeria). J Entomol Zool Stud (2016) 4:391–8.
Keywords: Aedes, breeding, habitat, physicochemical characteristic, Kinshasa (DRC)
Citation: Mbanzulu KM, Mboera LEG, Wumba R, Engbu D, Bojabwa MM, Zanga J, Mitashi PM, Misinzo G and Kimera SI (2022) Physicochemical Characteristics of Aedes Mosquito Breeding Habitats in Suburban and Urban Areas of Kinshasa, Democratic Republic of the Congo. Front. Trop. Dis 2:789273. doi: 10.3389/fitd.2021.789273
Received: 04 October 2021; Accepted: 16 December 2021;
Published: 19 January 2022.
Edited by:Chelsea T. Smartt, University of Florida, United States
Copyright © 2022 Mbanzulu, Mboera, Wumba, Engbu, Bojabwa, Zanga, Mitashi, Misinzo and Kimera. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Kennedy Makola Mbanzulu, firstname.lastname@example.org