The Risk of Dengue Virus Transmission in Dar es Salaam, Tanzania during an Epidemic Period of 2014

Leonard E G Mboera, Clement N Mweya, Susan F Rumisha, Patrick K Tungu, Grades Stanley, Mariam R Makange, Gerald Misinzo, Pasquale De Nardo, Francesco Vairo, Ndekya M Oriyo, Leonard E G Mboera, Clement N Mweya, Susan F Rumisha, Patrick K Tungu, Grades Stanley, Mariam R Makange, Gerald Misinzo, Pasquale De Nardo, Francesco Vairo, Ndekya M Oriyo

Abstract

Background: In 2010, 2012, 2013 and 2014 dengue outbreaks have been reported in Dar es Salaam, Tanzania. However, there is no comprehensive data on the risk of transmission of dengue in the country. The objective of this study was to assess the risk of transmission of dengue in Dar es Salaam during the 2014 epidemic.

Methodology/principal findings: This cross-sectional study was conducted in Dar es Salaam, Tanzania during the dengue outbreak of 2014. The study involved Ilala, Kinondoni and Temeke districts. Adult mosquitoes were collected using carbon dioxide-propane powered Mosquito Magnet Liberty Plus traps. In each household compound, water-holding containers were examined for mosquito larvae and pupae. Dengue virus infection of mosquitoes was determined using real-time reverse transcription polymerase chain reaction (qRT-PCR). Partial amplification and sequencing of dengue virus genome in infected mosquitoes was performed. A total of 1,000 adult mosquitoes were collected. Over half (59.9%) of the adult mosquitoes were collected in Kinondoni. Aedes aegypti accounted for 17.2% of the mosquitoes of which 90.6% were from Kinondoni. Of a total of 796 houses inspected, 38.3% had water-holding containers in their premises. Kinondoni had the largest proportion of water-holding containers (57.7%), followed by Temeke (31.4%) and Ilala (23.4%). The most common breeding containers for the Aedes mosquitoes were discarded plastic containers and tires. High Aedes infestation indices were observed for all districts and sites, with a house index of 18.1% in Ilala, 25.5% in Temeke and 35.3% in Kinondoni. The respective container indices were 77.4%, 65.2% and 80.2%. Of the reared larvae and pupae, 5,250 adult mosquitoes emerged, of which 61.9% were Ae. aegypti. Overall, 27 (8.18) of the 330 pools of Ae. aegypti were positive for dengue virus. On average, the overall maximum likelihood estimate (MLE) indicates pooled infection rate of 8.49 per 1,000 mosquitoes (95%CI = 5.72-12.16). There was no significant difference in pooled infection rates between the districts. Dengue viruses in the tested mosquitoes clustered into serotype 2 cosmopolitan genotype.

Conclusions/significance: Ae. aegypti is the main vector of dengue in Dar es Salaam and breeds mainly in medium size plastic containers and tires. The Aedes house indices were high, indicating that the three districts were at high risk of dengue transmission. The 2014 dengue outbreak was caused by Dengue virus serotype 2. The high mosquito larval and pupal indices in the area require intensification of vector surveillance along with source reduction and health education.

Conflict of interest statement

The authors have declared that no competing interest exist.

Figures

Fig 1. Study districts and sites in…
Fig 1. Study districts and sites in Dar es Salaam.
Fig 2. Average productivity of the mosquito…
Fig 2. Average productivity of the mosquito larvae (A) and pupae (B) per type of water-holding container separating those found with larvae/pupae and all inspected.
Fig 3. Neighbor-joining tree depicting the four…
Fig 3. Neighbor-joining tree depicting the four serotypes of dengue virus.
Dengue virus in mosquitoes collected in Dar es Salaam (indicated in bold) clustered into serotype 2. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) is shown adjacent to the nodes.

References

    1. Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL (2013) The global distribution and burden of dengue. Nature 496: 504–507. 10.1038/nature12060
    1. WHO (2009) Dengue: Guidelines for diagnosis, treatment, prevention and control World Health Organisation, Geneva, Switzerland.
    1. Amarasinghe A, Kuritsk JN, Letson GW, Margolis HS (2011) Dengue virus infection in Africa. Emerg Infect Dis 17: 1349–1354. 10.3201/eid1708.101515
    1. Gubler DJ (1997) Dengue and dengue haemorrhagic fever: its history and resurgence as global public health problem In: Gubler DJ, Kuno G, editors. Dengue and Dengue Hemorrhagic Fever. CAB International, Walkingford, UK: pp. 1–22.
    1. Sang RC (2007) Dengue in Africa. In: Report of the scientific working group meeting on dengue. Geneva, October 1–5, 2006. WHO Special Programme for Research and Training in Tropical Diseases; 2007. pp. 50–2 [cited 2011 April 13]. .
    1. LeDuc JW, Esteves K, Gratz NG (2004) Dengue and dengue haemorrhagic fever In: Murray CJ, Lopez AD, Mathers CD, editors. The Global Epidemiology of Infectious Diseases. Vol IV Global Burden of Disease and Injury Series Geneva: World Health Organization; pp. 219–242.
    1. Christie J (1872) Remarks on "Kidinga Pepo": A Peculiar Form of Exanthematous Disease. Br Med J 1: 577–579.
    1. Halstead SB (2008) Dengue: overview and history In: Halstead SB, editors. Dengue. London: Imperial College Press; pp. 1–28.
    1. Vairo F, Nicastri E, Meschi S, Schepisi MS, Paglia MG, Bevilacqua N, et al. (2012) Seroprevalence of dengue infection: a cross-sectional survey in mainland Tanzania and on Pemba Island, Zanzibar. Int J Infect Dis 16: e44–e46. S1201-9712(11)00202-5 [pii] 10.1016/j.ijid.2011.09.018
    1. Vairo F, Nicastri E, Yussuf SM, Cannas A, Meschi S, Mahmoud MA, et al. (2014) IgG against dengue virus in healthy blood donors, Zanzibar, Tanzania. Emerg Infect Dis 20: 465–468. 10.3201/eid2003.130150
    1. Weller N, Clowes P, Dobler G, Saathoff E, Kroidl I, Ntinginya NE, et al. (2014) Seroprevalence of alphavirus antibodies in a cross-sectional study in southwestern Tanzania suggests endemic circulation of chikungunya. PLoS Negl Trop Dis 8: e2979 PNTD-D-13-01890 [pii]. 10.1371/journal.pntd.0002979
    1. WHO (2011) Comprehensive Guidelines for Prevention and Control of Dengue and Dengue Haemorrhagic Fever. Revised and Expanded Edition. SEARO Technical Publication Series No. 60.
    1. URT (2013) Population and housing census 2012: Population distribution by administrative units Volume 1 National Bureau of Statistics.The United Republic of Tanzania; Dar es Salaam.
    1. Trpis M (1972) Seasonal changes in the larval populations of Aedes aegypti in two biotopes in Dar es Salaam, Tanzania. Bull World Health Organ 47: 245–255.
    1. Huang YM (2001) A pictorial key for the identification of the subfamilies of Culicidae, genera of Culicinae, and subgenera of Aedes mosquitoes of the Afrotropical Region (Diptera: Culicidae). Proceedings of the Entomological Society of Washington 103: 1–53.
    1. Domingo C, Niedrig M, Teichmann A, Kaiser M, Rumer L, Jarman RG, et al. (2010) 2nd International external quality control assessment for the molecular diagnosis of dengue infections. PLoS Negl Trop Dis 4.
    1. Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV (1992) Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J Clin Microbiol 30: 545–551.
    1. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731–2739. msr121 [pii]. 10.1093/molbev/msr121
    1. Biggerstaff B (2005) PooledInfRate software. Vector Borne Zoonotic Dis 5: 420–421.
    1. Trpis M (1972) Dry season survival of Aedes aegypti eggs in various breeding sites in the Dar es Salaam area, Tanzania. Bull World Health Organ 47: 433–437.
    1. Rao TR, Trpis M, Gillett JD, Teesdale C, Tonn RJ (1973) Breeding places and seasonal incidence of Aedes aegypti, as assessed by the single-larva survey method. Bull World Health Organ 48: 615–622.
    1. Moore CG, Cline BL, Ruiz-Tiben E, Lee D, Romney-Joseph H, Rivera-Correa E (1978) Aedes aegypti in Puerto Rico: environmental determinants of larval abundance and relation to dengue virus transmission. Am J Trop Med Hyg 27: 1225–1231.
    1. Trpis M (1972) Breeding of Aedes aegypti and A. simpsoni under the escarpment of the Tanzanian plateau. Bull World Health Organ 47: 77–82.
    1. Focks DA, Chadee DD (1997) Pupal survey: an epidemiologically significant surveillance method for Aedes aegypti: an example using data from Trinidad. Am J Trop Med Hyg 56: 159–167.
    1. David MR, Lourenco-de-Oliveira R, Freitas RM (2009) Container productivity, daily survival rates and dispersal of Aedes aegypti mosquitoes in a high income dengue epidemic neighbourhood of Rio de Janeiro: presumed influence of differential urban structure on mosquito biology. Mem Inst Oswaldo Cruz 104: 927–932. S0074-02762009000600019 [pii].
    1. Sanchez L, Vanlerberghe V, Alfonso L, Marquetti MC, Guzman MG, Bisset J, et al. (2006) Aedes aegypti larval indices and risk for dengue epidemics. Emerg Infect Dis 12: 800–806.
    1. Goh KT, Ng SK, Chan YC, Lim SJ, Chua EC (1987) Epidemiological aspects of an outbreak of dengue fever/dengue haemorrhagic fever in Singapore. Southeast Asian J Trop Med Public Health 18: 295–302.
    1. Maciel-de-Freitas R, Marques WA, Peres RC, Cunha SP, de Oliveira RL (2007) Variation in Aedes aegypti (Diptera: Culicidae) container productivity in a slum and a suburban district of Rio de Janeiro during dry and wet seasons. Mem Inst Oswaldo Cruz 102: 489–496. S0074-02762007000400010 [pii].
    1. Appawu M, Dadzie S, Abdul H, Asmah H, Boakye D, Wilson M, et al. (2006) Surveillance of viral haemorrhagic fevers in ghana: entomological assessment of the risk of transmission in the northern regions. Ghana Med J 40: 137–141.
    1. Getis A, Morrison AC, Gray K, Scott TW (2003) Characteristics of the spatial pattern of the dengue vector, Aedes aegypti, in Iquitos, Peru. Am J Trop Med Hyg 69: 494–505.
    1. Morrison AC, Getis A, Santiago M, Rigau-Perez JG, Reiter P (1998) Exploratory space-time analysis of reported dengue cases during an outbreak in Florida, Puerto Rico, 1991–1992. Am J Trop Med Hyg 58: 287–298.
    1. Neff JM, Morris L, Gonzalez-Alcover R, Coleman PH, Lyss SB, Negron H (1967) Dengue fever in a Puerto Rican community. Am J Epidemiol 86: 162–184.
    1. Tun-Lin W, Kay BH, Barnes A (1995) Understanding productivity, a key to Aedes aegypti surveillance. Am J Trop Med Hyg 53: 595–601.
    1. Waterman SH, Novak RJ, Sather GE, Bailey RE, Rios I, Gubler DJ (1985) Dengue transmission in two Puerto Rican communities in 1982. Am J Trop Med Hyg 34: 625–632.
    1. Garcia-Rejon J, Lorono-Pino MA, Farfan-Ale JA, Flores-Flores L, Del PR-P, Rivero-Cardenas N, et al. (2008) Dengue virus-infected Aedes aegypti in the home environment. Am J Trop Med Hyg 79: 940–950. 79/6/940 [pii].
    1. Ritchie SA, Pyke AT, Hall-Mendelin S, Day A, Mores CN, Christofferson RC, et al. (2013) An explosive epidemic of DENV-3 in Cairns, Australia. PLoS One 8: e68137 PONE-D-13-12209 [pii]. 10.1371/journal.pone.0068137
    1. Yoon IK, Getis A, Aldstadt J, Rothman AL, Tannitisupawong D, Koenraadt CJ, et al. (2012) Fine scale spatiotemporal clustering of dengue virus transmission in children and Aedes aegypti in rural Thai villages. PLoS Negl Trop Dis 6: e1730 1. PNTD-D-12-00340 [pii]. 10.1371/journal.pntd.0001730
    1. Mammen MP, Pimgate C, Koenraadt CJ, Rothman AL, Aldstadt J, Nisalak A, et al. (2008) Spatial and temporal clustering of dengue virus transmission in Thai villages. PLoS Med 5: e205 08-PLME-RA-0417 [pii] 10.1371/journal.pmed.0050205
    1. Garcia-Rejon JE, Lorono-Pino MA, Farfan-Ale JA, Flores-Flores LF, Lopez-Uribe MP, Najera-Vazquez MR, et al. (2011) Mosquito infestation and dengue virus infection in Aedes aegypti females in schools in Merida, Mexico. Am J Trop Med Hyg 84: 489–496. 84/3/489 [pii] 10.4269/ajtmh.2011.10-0654
    1. Schafrick NH, Milbrath MO, Berrocal VJ, Wilson ML, Eisenberg JN (2013) Spatial clustering of Aedes aegypti related to breeding container characteristics in Coastal Ecuador: implications for dengue control. Am J Trop Med Hyg 89: 758–765. ajtmh.12-0485 [pii] 10.4269/ajtmh.12-0485
    1. Duncombe J, Clements A, Davis J, Hu W, Weinstein P, Ritchie S (2013) Spatiotemporal patterns of Aedes aegypti populations in Cairns, Australia: assessing drivers of dengue transmission. Trop Med Int Health 18: 839–849. 10.1111/tmi.12115
    1. Kroeger A, Lenhart A, Ochoa M, Villegas E, Levy M, Alexander N, et al. (2006) Effective control of dengue vectors with curtains and water container covers treated with insecticide in Mexico and Venezuela: cluster randomised trials. BMJ 332: 1247–1252. 332/7552/1247 [pii]
    1. Stoddard ST, Forshey BM, Morrison AC, Paz-Soldan VA, Vazquez-Prokopec GM, Astete H, et al. (2013) House-to-house human movement drives dengue virus transmission. Proc Natl Acad Sci USA 110: 994–999. 1213349110 [pii] 10.1073/pnas.1213349110
    1. Stoddard ST, Morrison AC, Vazquez-Prokopec GM, Paz S, V, Kochel TJ, Kitron U, et al. (2009) The role of human movement in the transmission of vector-borne pathogens. PLoS Negl Trop Dis 3: e481 10.1371/journal.pntd.0000481
    1. Moi ML, Takasaki T, Kotaki A, Tajima S, Lim CK, Sakamoto M, et al. (2010) Importation of dengue virus type 3 to Japan from Tanzania and Cote d'Ivoire. Emerg Infect Dis 16: 1770–1772. 10.3201/eid1611.101061
    1. Das B, Hazra RK (2013) Entomological investigation with special attention to pupal indicators of Aedes vectors during outbreaks of dengue in coastal Odisha, India. J Vector Borne Dis 50: 147–150.

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