Skip to main content
Top
Published in: Virology Journal 1/2020

Open Access 01-12-2020 | Dengue Virus | Research

Association of genotype III of dengue virus serotype 3 with disease outbreak in Eastern Sudan, 2019

Authors: Mawahib H. Eldigail, Hazem A. Abubaker, Fatima A. Khalid, Tajeldin M. Abdallah, Hassan H. Musa, Mohamed E. Ahmed, Gamal K. Adam, Mustafa I. Elbashir, Imadeldin E. Aradaib

Published in: Virology Journal | Issue 1/2020

Login to get access

Abstract

Background

Dengue fever (DF) is an arthropod-borne disease caused by dengue virus (DENV). DENV is a member of the genus Flavivirus in the family Flaviviridae. Recently, DENV has been reported as an important emerging infectious viral pathogen in Sudan. Multiple outbreaks and sporadic cases of DF have been frequently reported in the eastern region of Sudan. The present study was conducted to confirm DENV outbreak in Kassala State, eastern Sudan, 2019, and to provide some information on the molecular characterization of the DENV isolate associated with the disease outbreak.

Methods

A hundred serum samples were collected during the outbreak from residents of Kassala State, Sudan, 2019. ELISA was used to detect DENV non structural protein NS1 (DENV-NS1) in acute phase sera sampled during the disease outbreak. RT-PCR assays were used to amplify a fragment of the capsid/pre-membrane region (CprM) of the viral polyprotein gene. The PCR products of the amplified CprM region of the viral polyprotein gene were purified and partial sequences were generated and used to confirm the specificity of DENV sequences and to identify the virus serotype. Phylogenetic tree was constructed to determine the genotype of DENV associated with the outbreak.

Results

Using DENV-NS1 ELISA assay, DENV infection was confirmed in 23% sampled sera. The detection of DENV RNA was made possible using group-specific RT-PCR assay. The virus was serotyped as DENV serotype 3 (DENV-3) using DENV serotype-specific RT-PCR assay. Phylogenetic analysis of the partial CprM sequences of the viral polyprotein gene indicates that the virus belonged to genotype III of DENV-3.

Conclusion

The scientific data presented in this investigation confirmed that genotype III of DENV-3 was associated with the disease outbreak in eastern Sudan, 2019. The study represents the first report on molecular characterization of DENV-3 in Sudan.
Literature
1.
go back to reference Amarasinghe A, Kuritsky JN, Letson GW, Margolis HS. Dengue virus infection inAfrica. Emerg Infect Dis. 2011;17:1349–54.PubMedPubMedCentral Amarasinghe A, Kuritsky JN, Letson GW, Margolis HS. Dengue virus infection inAfrica. Emerg Infect Dis. 2011;17:1349–54.PubMedPubMedCentral
2.
go back to reference Azhar EI, Hashem AM, El-Kafrawy SA, Abol-Ela S, Abd-Alla AM, Sohrab SS, et al. Complete genome sequencing and phylogenetic analysis of dengue type 1 virus isolated from Jeddah, Saudi Arabia. Virol J. 2015;12:1.CrossRef Azhar EI, Hashem AM, El-Kafrawy SA, Abol-Ela S, Abd-Alla AM, Sohrab SS, et al. Complete genome sequencing and phylogenetic analysis of dengue type 1 virus isolated from Jeddah, Saudi Arabia. Virol J. 2015;12:1.CrossRef
3.
go back to reference Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, et al. The global distribution and burden of dengue. Nature. 2013;496:504–7.CrossRef Bhatt S, Gething PW, Brady OJ, Messina JP, Farlow AW, Moyes CL, Drake JM, Brownstein JS, Hoen AG, Sankoh O, et al. The global distribution and burden of dengue. Nature. 2013;496:504–7.CrossRef
4.
go back to reference Brady OJ, Gething PW, Bhatt S, Messina JP, Brownstein JS, Hoen AG, Moyes CL, Farlow AW, Scott TW, Hay SI. Refining the global spatial limits of dengue virus transmission by evidence-based consensus. PLoS Negl Trop Dis. 2012;6:e1760.CrossRef Brady OJ, Gething PW, Bhatt S, Messina JP, Brownstein JS, Hoen AG, Moyes CL, Farlow AW, Scott TW, Hay SI. Refining the global spatial limits of dengue virus transmission by evidence-based consensus. PLoS Negl Trop Dis. 2012;6:e1760.CrossRef
5.
go back to reference Kanesa-Thasan N, Chang GJ, Smoak BL, Magill A, Burrous MJ, HokeJr CH. Molecular and epidemiologic analysis of dengue virus isolates from Somalia. Emerg Infect Dis. 1998;4:299–303.CrossRef Kanesa-Thasan N, Chang GJ, Smoak BL, Magill A, Burrous MJ, HokeJr CH. Molecular and epidemiologic analysis of dengue virus isolates from Somalia. Emerg Infect Dis. 1998;4:299–303.CrossRef
6.
go back to reference Gubler DJ. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol. 2002;10:100–3.CrossRef Gubler DJ. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol. 2002;10:100–3.CrossRef
7.
go back to reference Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, Hunsperger E, Kroeger A, Margolis HS, Martínez E, et al. Dengue: a continuing global threat. Nat Rev Microbiol. 2010;8:S7–S16.CrossRef Guzman MG, Halstead SB, Artsob H, Buchy P, Farrar J, Gubler DJ, Hunsperger E, Kroeger A, Margolis HS, Martínez E, et al. Dengue: a continuing global threat. Nat Rev Microbiol. 2010;8:S7–S16.CrossRef
8.
go back to reference Loroño-Pino MA, Cropp CB, Farfán JA, Vorndam AV, Rodriguez-Angulo EM, Rosado-Paredes EP, et al. Common occurrence of concurrent infections by multiple dengue virus serotypes. Am J Trop Med Hyg. 1999;61:725–30.CrossRef Loroño-Pino MA, Cropp CB, Farfán JA, Vorndam AV, Rodriguez-Angulo EM, Rosado-Paredes EP, et al. Common occurrence of concurrent infections by multiple dengue virus serotypes. Am J Trop Med Hyg. 1999;61:725–30.CrossRef
9.
go back to reference Adam A, Schüttoff T, Reiche S, Jassoy C. High seroprevalence of dengue virus indicates that dengue virus infections are frequent in central and eastern Sudan. Tropical Med Int Health. 2018;23:960–7.CrossRef Adam A, Schüttoff T, Reiche S, Jassoy C. High seroprevalence of dengue virus indicates that dengue virus infections are frequent in central and eastern Sudan. Tropical Med Int Health. 2018;23:960–7.CrossRef
10.
go back to reference Elduma AH, Osman WM. Dengue and hepatitis E virus infection in pregnant women in eastern Sudan, a challenge for diagnosis in an endemic area. Pan Afr Med J. 2014;19:391.CrossRef Elduma AH, Osman WM. Dengue and hepatitis E virus infection in pregnant women in eastern Sudan, a challenge for diagnosis in an endemic area. Pan Afr Med J. 2014;19:391.CrossRef
11.
go back to reference Soghaier MA, Himatt S, Osman KE, Okoued SI, Seidahmed OE, Beatty ME, Elmusharaf K, Khogali J, Shingrai NH, Elmangory MM. Cross-sectional community-based study of the socio-demographic factors associated with the prevalence of dengue in the eastern part of Sudan in 2011. BMC Public Health. 2015;15:558.CrossRef Soghaier MA, Himatt S, Osman KE, Okoued SI, Seidahmed OE, Beatty ME, Elmusharaf K, Khogali J, Shingrai NH, Elmangory MM. Cross-sectional community-based study of the socio-demographic factors associated with the prevalence of dengue in the eastern part of Sudan in 2011. BMC Public Health. 2015;15:558.CrossRef
12.
go back to reference Soghaier MA, Mahmood SF, Pasha O, Azam SI, Karsani MM, Elmangory MM, Elmagboul BA, Okoued SI, Shareef SM, Khogali HS, Eltigai E. Factors associated with dengue fever IgGsero-prevalence in South Kordofan state, Sudan,in 2012: reporting prevalence ratios. J Infect Public Health. 2014;7:54–61.CrossRef Soghaier MA, Mahmood SF, Pasha O, Azam SI, Karsani MM, Elmangory MM, Elmagboul BA, Okoued SI, Shareef SM, Khogali HS, Eltigai E. Factors associated with dengue fever IgGsero-prevalence in South Kordofan state, Sudan,in 2012: reporting prevalence ratios. J Infect Public Health. 2014;7:54–61.CrossRef
13.
go back to reference Abdallah TM, Ali AAA, Karsany MS, Adam I. Epidemiology of dengue infections in Kassala, Eastern Sudan. J Med Virol. 2012;84:500–3.CrossRef Abdallah TM, Ali AAA, Karsany MS, Adam I. Epidemiology of dengue infections in Kassala, Eastern Sudan. J Med Virol. 2012;84:500–3.CrossRef
14.
go back to reference Himatt S, Osman KE, Okoued SI, Seidahmed OE, Beatty ME, Soghaier MA, Elmusharaf K. Sero-prevalence of dengue infections in the Kassala state in the eastern part of the Sudan in 2011. J Infect Public Health. 2015;8:487–92.CrossRef Himatt S, Osman KE, Okoued SI, Seidahmed OE, Beatty ME, Soghaier MA, Elmusharaf K. Sero-prevalence of dengue infections in the Kassala state in the eastern part of the Sudan in 2011. J Infect Public Health. 2015;8:487–92.CrossRef
15.
go back to reference Noureldin E, Shaffer L. Role of climatic factors in the incidence of dengue in Port Sudan City, Sudan. East Mediterr Health J. 2019;25:852–60.CrossRef Noureldin E, Shaffer L. Role of climatic factors in the incidence of dengue in Port Sudan City, Sudan. East Mediterr Health J. 2019;25:852–60.CrossRef
16.
go back to reference Hyams KC, Oldfield EC, Scott RM, Bourgeois AL, Gardiner H, Pazzaglia G, Moussa M, Saleh AS, Dawi OE, Daniell FD. Evaluation of febrile patients in Port Sudan, Sudan: isolation of dengue virus. Am J Trop Med Hyg. 1986;35:860–5.CrossRef Hyams KC, Oldfield EC, Scott RM, Bourgeois AL, Gardiner H, Pazzaglia G, Moussa M, Saleh AS, Dawi OE, Daniell FD. Evaluation of febrile patients in Port Sudan, Sudan: isolation of dengue virus. Am J Trop Med Hyg. 1986;35:860–5.CrossRef
17.
go back to reference Hamid Z, Hamid T, Alsedig K, Abdallah T, Elaagip A, Ahmed A, Khalid F, Abdel HM. Molecular investigation of dengue virus serotype 2 circulation in Kassala state, Sudan. Jpn J Infect Dis. 2019;72:58–61.CrossRef Hamid Z, Hamid T, Alsedig K, Abdallah T, Elaagip A, Ahmed A, Khalid F, Abdel HM. Molecular investigation of dengue virus serotype 2 circulation in Kassala state, Sudan. Jpn J Infect Dis. 2019;72:58–61.CrossRef
18.
go back to reference Eldigail MH, Adam GK, Babiker RA, Khalid F, Adam IA, Omer OH, Ahmed ME, Birair SL, Haroun EM, AbuAisha H, Karrar AE, Abdalla HS, Aradaib IE. Prevalence of dengue fever virus antibodies and associated risk factors among residents of El-Gadarif state, Sudan. BMC Public Health. 2018;18:921.CrossRef Eldigail MH, Adam GK, Babiker RA, Khalid F, Adam IA, Omer OH, Ahmed ME, Birair SL, Haroun EM, AbuAisha H, Karrar AE, Abdalla HS, Aradaib IE. Prevalence of dengue fever virus antibodies and associated risk factors among residents of El-Gadarif state, Sudan. BMC Public Health. 2018;18:921.CrossRef
19.
go back to reference Cummings DAT, Irizarry RA, Huang NE, Endy TP, Nisalak A, Ungchusak K, Burke DS. Travelling waves in the occurrence of dengue hemorrhagic fever in Thailand. Nature. 2004;427:344–7.CrossRef Cummings DAT, Irizarry RA, Huang NE, Endy TP, Nisalak A, Ungchusak K, Burke DS. Travelling waves in the occurrence of dengue hemorrhagic fever in Thailand. Nature. 2004;427:344–7.CrossRef
20.
go back to reference Wesolowski A, Qureshi T, Boni MF, Sundsøy PR, Johansson MA, Rasheed SB, Engø-Monsen K, Buckee CO. Impact of human mobility on the emergence of dengue epidemics in Pakistan. Proc Natl Acad Sci U S A. 2015;112:11887–92.CrossRef Wesolowski A, Qureshi T, Boni MF, Sundsøy PR, Johansson MA, Rasheed SB, Engø-Monsen K, Buckee CO. Impact of human mobility on the emergence of dengue epidemics in Pakistan. Proc Natl Acad Sci U S A. 2015;112:11887–92.CrossRef
21.
22.
go back to reference Wilder-Smith A, Gubler DJ. Geographic expansion of dengue: the impact of international travel. Med Clin. 2008;92:1377–90. Wilder-Smith A, Gubler DJ. Geographic expansion of dengue: the impact of international travel. Med Clin. 2008;92:1377–90.
23.
go back to reference Seidahmed OM, Hassan SA, Soghaier MA, Siam HA, Ahmed FT, Elkarsany MM, Sulaiman SM. Spatial and temporal patterns of dengue transmission along a Red Sea coastline: a longitudinal entomological and serological survey in Port Sudan city. PLoS Negl Trop Dis. 2012;6:e1821.CrossRef Seidahmed OM, Hassan SA, Soghaier MA, Siam HA, Ahmed FT, Elkarsany MM, Sulaiman SM. Spatial and temporal patterns of dengue transmission along a Red Sea coastline: a longitudinal entomological and serological survey in Port Sudan city. PLoS Negl Trop Dis. 2012;6:e1821.CrossRef
24.
go back to reference Tatem AJ, Hay SI, Rogers DJ. Global traffic and disease vector dispersal. Proc Natl Acad Sci U S A. 2006;103:6242–7.CrossRef Tatem AJ, Hay SI, Rogers DJ. Global traffic and disease vector dispersal. Proc Natl Acad Sci U S A. 2006;103:6242–7.CrossRef
26.
go back to reference Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV. Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J Clin Microbiol. 1992;30:545–51.CrossRef Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV. Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J Clin Microbiol. 1992;30:545–51.CrossRef
27.
go back to reference Konongoi L, Ofula V, Nyunja A, Owaka S, Koka H, Makio A, Koskei E, Eyase F, Langat D, Schoepp RJ, Rossi CA, Njeru I, Coldren R, Sang R. Detection of dengue virus serotypes 1, 2 and 3 in selected regions of Kenya: 2011-2014. Virol J. 2016;13:182.CrossRef Konongoi L, Ofula V, Nyunja A, Owaka S, Koka H, Makio A, Koskei E, Eyase F, Langat D, Schoepp RJ, Rossi CA, Njeru I, Coldren R, Sang R. Detection of dengue virus serotypes 1, 2 and 3 in selected regions of Kenya: 2011-2014. Virol J. 2016;13:182.CrossRef
30.
go back to reference McCarthy MC, Haberberger RL, Salib AW, Soliman BA, El-Tigani A, Khalid IO, Watts DM. Evaluation of arthropod-borne viruses and other infectious disease pathogens as the causes of febrile illnesses in the Khartoum Province of Sudan. J Med Virol. 1996;48:141–6.CrossRef McCarthy MC, Haberberger RL, Salib AW, Soliman BA, El-Tigani A, Khalid IO, Watts DM. Evaluation of arthropod-borne viruses and other infectious disease pathogens as the causes of febrile illnesses in the Khartoum Province of Sudan. J Med Virol. 1996;48:141–6.CrossRef
31.
go back to reference Seidahmed OM, Siam HA, Soghaier MA, Abubakr M, Osman HA, AbdElrhman LS, Elmagbol B, Velayudhan R. Dengue vector control and surveillance during a major outbreak in a coastal Red Sea area in Sudan. East Mediterr Health J. 2012;18:1217–24.CrossRef Seidahmed OM, Siam HA, Soghaier MA, Abubakr M, Osman HA, AbdElrhman LS, Elmagbol B, Velayudhan R. Dengue vector control and surveillance during a major outbreak in a coastal Red Sea area in Sudan. East Mediterr Health J. 2012;18:1217–24.CrossRef
32.
go back to reference Balmaseda A, Hammond SN, Perez L, Tellez Y, Saborio SI, Mercado JC, et al. Serotype-specific differences in clinical manifestations of dengue. Am J Trop Med Hyg. 2006;74:449–56.CrossRef Balmaseda A, Hammond SN, Perez L, Tellez Y, Saborio SI, Mercado JC, et al. Serotype-specific differences in clinical manifestations of dengue. Am J Trop Med Hyg. 2006;74:449–56.CrossRef
33.
go back to reference Malik A, Earhart K, Mohareb E, Saad M, Saeed M, Ageep A, Soliman A. Dengue hemorrhagic fever outbreak in children in Port Sudan. J Infect Public Health. 2011;4:1–6.CrossRef Malik A, Earhart K, Mohareb E, Saad M, Saeed M, Ageep A, Soliman A. Dengue hemorrhagic fever outbreak in children in Port Sudan. J Infect Public Health. 2011;4:1–6.CrossRef
34.
go back to reference Jelinek T. Dengue fever in international travelers. Clin Infect Dis. 2000;31:144–7.CrossRef Jelinek T. Dengue fever in international travelers. Clin Infect Dis. 2000;31:144–7.CrossRef
35.
go back to reference Stoddard ST, Morrison AC, Vazquez-Prokopec GM, Soldan VP, Kochel TJ, Kitron U, Elder JP, Scott TW. The Role of Human Movement in the Transmission of Vector-Borne Pathogens. PLoS Neg. Trop. Dis. 2009;3:e481.CrossRef Stoddard ST, Morrison AC, Vazquez-Prokopec GM, Soldan VP, Kochel TJ, Kitron U, Elder JP, Scott TW. The Role of Human Movement in the Transmission of Vector-Borne Pathogens. PLoS Neg. Trop. Dis. 2009;3:e481.CrossRef
36.
go back to reference Liebig J, Jansen C, Paini D, Gardner L, Jurdak R. A global model for predicting the arrival of imported dengue infections. PLoS One. 2019;14:e0225193.CrossRef Liebig J, Jansen C, Paini D, Gardner L, Jurdak R. A global model for predicting the arrival of imported dengue infections. PLoS One. 2019;14:e0225193.CrossRef
37.
go back to reference Gubler DJ. Dengue, urbanization and globalization: the unholy trinity of the 21st century. Trop Med Health. 2011;39:3–11.CrossRef Gubler DJ. Dengue, urbanization and globalization: the unholy trinity of the 21st century. Trop Med Health. 2011;39:3–11.CrossRef
38.
go back to reference Sierra B, Kouri G, Guzman MG. Race: a risk factor for dengue hemorrhagic fever. Arch Virol. 2007;152:533–42.CrossRef Sierra B, Kouri G, Guzman MG. Race: a risk factor for dengue hemorrhagic fever. Arch Virol. 2007;152:533–42.CrossRef
39.
go back to reference Chepkorir E, Lutomiah J, Mutisya J, Mulwa F, Limbaso K, Orindi B, et al. Vector competence of Aedesaegypti populations from Kilifi and Nairobi for dengue 2 virus and the influence of temperature. Parasit Vectors. 2014;7. Chepkorir E, Lutomiah J, Mutisya J, Mulwa F, Limbaso K, Orindi B, et al. Vector competence of Aedesaegypti populations from Kilifi and Nairobi for dengue 2 virus and the influence of temperature. Parasit Vectors. 2014;7.
40.
go back to reference Simmons CP, Farrar JJ, van VinhChau N, Wills B. Dengue. N Engl J Med. 2012;366:1423–32.CrossRef Simmons CP, Farrar JJ, van VinhChau N, Wills B. Dengue. N Engl J Med. 2012;366:1423–32.CrossRef
Metadata
Title
Association of genotype III of dengue virus serotype 3 with disease outbreak in Eastern Sudan, 2019
Authors
Mawahib H. Eldigail
Hazem A. Abubaker
Fatima A. Khalid
Tajeldin M. Abdallah
Hassan H. Musa
Mohamed E. Ahmed
Gamal K. Adam
Mustafa I. Elbashir
Imadeldin E. Aradaib
Publication date
01-12-2020
Publisher
BioMed Central
Keyword
Dengue Virus
Published in
Virology Journal / Issue 1/2020
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-020-01389-9

Other articles of this Issue 1/2020

Virology Journal 1/2020 Go to the issue