Zarroug et al. BMC Infectious Diseases          (2019) 19:477 
https://doi.org/10.1186/s12879-019-4113-1
RESEARCH ARTICLE Open Access
Notes on distribution of Simulium
damnosum s. l. along Atbara River in
Galabat sub-focus, eastern Sudan
Isam M. A. Zarroug1*, Arwa Elaagip2, Suhaib G. Gumaa3, Altayeb K. Ali4, Ayman Ahmed5, Hanaa A. M. Siam5,
Deena M. Abdelgadir6, Olabanji A. Surakat7, Olatunwa J. Olamiju8, Daniel A. Boakye9, Nabil Aziz10 and
Kamal Hashim11
Abstract
Background: Onchocerciasis is caused by a nematode worm Onchocerca volvulus, which is transmitted in Sudan by
black fly vectors of the Simulium damnosum sensu lato species complex. In Sudan, the disease is found in four foci
where fast flowing rivers provide suitable breeding sites for the Simulium vector flies. The construction of dams and
irrigation schemes for agricultural purposes has affected black fly breeding and distribution, such as in Merowe
Dam in Abu-Hamed focus, where the perennially flowing water downstream of the Dam created new vector
breeding sites, thereby, changing the pattern of disease transmission and creating public health problems. Based
on this situation, this study was carried out to measure the effect of the Upper Atbara and Setit Dam complex on
the distribution of Simulium damnosum s.l. breeding sites and on disease elimination in the Galabat sub-focus in
eastern Sudan.
Methods: Aquatic stages of Simulium were collected between October and November 2009, prior to the
construction of the dam complex, and again in 2013 and 2015 while the dam complex construction was ongoing.
Results: A total of 40 breeding sites were identified at the beginning of the study. After the construction of the
dam complex in 2015, seventeen previously mapped breeding sites were inaccessible as they had been flooded by
the dam complex’s lake when reach its maximum size. Three species were obtained from different locations: S.
damnosum s.l., S. griseicolle, and S. adersi.
Conclusions: This study has shown a link between the construction of the dam complex and a reduction in the
breeding sites of black fly vectors. This reduction has limited the Galabat sub-focus to a small area at the upper
Atbara River which become the end of the focus. To sustain the success achieved in onchocerciasis control in the
Galabat sub-focus, disease control and its vector control should be strengthened in the area cross-boarding Sudan
and Ethiopia.
Keywords: Upper Atbara dam, Setit dam, Dam complex, Simulium damnosum s.l., Distribution, Cross-border, Galabat
sub-focus, Eastern Sudan
* Correspondence: imazarroug@gmail.com
1Onchocerciasis Control/Elimination Programme, National Programme for
Prevention of Blindness (NPPB), Federal Ministry of Health, Khartoum, Sudan
Full list of author information is available at the end of the article
© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Zarroug et al. BMC Infectious Diseases          (2019) 19:477 Page 2 of 5
Background Metema sub-focus [17, 18]. It has been recommended
The River Nile is the longest river in the world [1]. The that any vector control activities based in this area
White Nile contributes a small amount to the annual would be operated by the Sudanese and Ethiopian gov-
flow discharge of the River Nile, but flows constantly ernments [17]. Galabat started full continuous annual
throughout the year. The Blue Nile and its tributaries community- directed treatment with ivermectin (CDTI)
contribute by high amount of annual flow but on a in 2007. The prevalence of microfilariae was determined
highly seasonal basis [1, 2]. Although the River Nile is in a previous survey as 63.4% associated with a remark-
the main source of water in Sudan, the River Atbara and able degree of pruritus and onchodermatitis [19]. The
its tributaries are of most importance as seasonal water corresponding black fly infectivity rate in Galabat was
streams, creating distinct environment for local commu- 6.9/10,000 flies (95% CI = 1.1–16.4) [18]. The man-biting
nities in eastern states [1]. activity of S. damnosum increased in September–De-
A recent construction began on the Upper Atbara and cember, then decreased in February–June. The highest
Setit Dam complex [1, 2]. This is a twin dam consisting vector density and monthly biting rates (MBR) were re-
of Rumela Dam on the Upper Atbara River and Burdana corded in September 2010 (N = 1163 flies, MBR = 6978
Dam on the Setit River in eastern Sudan. The dams are bites/person/month), whereas none were recorded from
located about 20 km upstream from the junction of the April to June. The hourly-based distribution of black
Atbara and Setit rivers and about 80 km to the south of flies showed a bimodal pattern with two peaks (07:00–
Khashm El-Girba Dam [1]. The project began in 2010 10:00) and (14:00–18:00) in the Galabat sub-focus [20].
and was finished in beginning of 2015. The two con- This study was conducted to document the breeding
nected dams have a joined reservoir. Their total length sites of onchocerciasis vector S. damnosum s.l. along At-
is 13 km [3]. bara River in the Galabat sub-focus, and to investigate
Black flies constitute a serious public health problem the effect of the construction of the dam complex on the
as vectors of human onchocerciasis and as a biting nuis- size of the sub-focus and the distribution of black fly
ance in many rural parts of the world [4, 5]. They breed vectors.
in rivers in a constant flow of fast-moving water where
they attach to rocks and plants and filter out suspended Methods
particles [5, 6]. Some human structures such as concrete Study area
dams and concrete-lined stream channels provide excel- The Galabat sub-focus is found in eastern Sudan around
lent developmental sites for larvae and pupae of black the Atbara River (N 14° 06`–12° 57`, E 35° 56`–36° 09`)
fly species. This may result in adverse environmental at an altitude range of 540–1040 m (Fig. 1). The water
and health impacts, which may extend to other coun- level at Atbara River increases generally in July to reach
tries, as in the case of the River Nile [5, 7, 8]. its peak in the rainy season from August to October,
In Sudan, human onchocerciasis is currently known in then decreases rapidly and forms isolated pools from
four main foci: Abu-Hamed in northern Sudan, Galabat March to May. The coordinates of each site from the
in eastern Sudan, Radom in southern Darfur in the first village in the sub-focus “Balashora” at the border
southwest, and Khor Yabus in Blue Nile region of the with Ethiopia to the last village in the sub-focus “Al Bah-
southeast [5]. Few studies have addressed the impact of kar” had been determined and listed in Additional file 1.
dams on transmission dynamics of onchocerciasis in Af-
rican countries [4, 9–12]. It has been suggested that on- Aquatic stages survey
chocerciasis is the major environmental health problem During 2009, 2013, and 2015, investigation of 40 Simu-
around other dams in Africa [5, 9, 13]. In Sudan, few lium breeding sites were conducted from October and
studies have highlighted the impact of dams on trans- November of each year during the study period (Add-
mission dynamics of onchocerciasis. Biting activity of itional file 1). After its construction in 2015, the area in
black flies was reported near Meridi and Roseires Dams, front of the dam complex was also surveyed for the
indicating that dam construction may affect the dynam- presence of the vectors.
ics and extent of onchocerciasis transmission [14, 15]. Aquatic stages (eggs, larvae, and pupae) of black flies
Additionally, larvae of S. damnsosum s.l. were found in were collected from different submerged plants like
the spillways of Khashm El-Girba Dam after its con- Digitaria ciliaris, Kanahia laniflora and Cynodon dacty-
struction [16]. Currently, Merowe Dam in Abu-Hamed lon which are locally known as Dees, Guweer, and
focus has effectively shrunken the focus to a little over Nageela respectively [21]. The collected larvae and
half of its original size and eliminated black fly breeding pupae were preserved in 80% ethyl alcohol for morpho-
sites west to the town of Abu-Hamed [5]. logical identification following the taxonomic keys of
The Galabat sub-focus is located along the banks of Freeman and de Meillon (1953), Crosskey (1962), Davies
Atbara River and extends to the Ethiopian land in the and Crosskey (1991) [22–24].
Zarroug et al. BMC Infectious Diseases          (2019) 19:477 Page 3 of 5
Fig. 1 Map of the Galabat sub-focus showing the study sites before and after the construction of the Upper Atbara and Setit Dam complex
Results Annual report of onchocerciasis in Galabat sub-focus/un-
Aquatic stages of Simulium black flies were collected from published], and the last breeding site was in Al Bahkar site
40 breeding sites in the Galabat sub-focus. Details of loca- in north of the focus (Fig. 1). After the construction of the
tions and abundance of breeding sites are described in dam complex in 2015, 17 breeding sites located from the
Additional file 1. Collected samples revealed three species: dam complex up to Um Gazaz site were totally flooded by
S. damnosum s.l. and two zoophilic species (S. griseicolle water of the dam complex’s lake, covering an area of more
and S. adersi). Immature stages of the zoophilic species than 100 km2 (Fig. 1). The 17 flooded sites were previously
were predominantly encountered downstream of Atbara known as breeding sites of onchocerciasis vectors (Add-
River, whereas, the S. damnosum s.l. was collected more itional file 1). Therefore, the first breeding site was found
from upstream of Atbara River where the fast current of near Wad Arood site (Fig. 1).
water with many rapids was clearly notable.
Before the construction of the dam complex, the first Discussion
breeding site for onchocerciasis vectors was found in Bala- Construction of dams has adverse effects on the physical
shora site near the Ethiopian border [APOC and NPPB: and biological environment [5, 9, 25]. In this study,
Zarroug et al. BMC Infectious Diseases          (2019) 19:477 Page 4 of 5
aquatic stages of Simulium black flies were collected from Additional file
40 breeding sites during 2009 and 2013. Clearly, the con-
struction of the Upper Atbara and Setit complex dam in Additional file 1: Abundance of aquatic stages of Simulium black fly
2015 has reduced the breeding sites of the vectors, as 17 collected from different sites in Galabat sub-focus, during 2009, 2013 and
2015. (DOCX 26 kb)
previous breeding sites were covered by flooded water
from the dam complex’s lake. This resulted in shrinking of Abbreviations
the Galabat sub-focus size. CDTI: Community-directed treatment with ivermectin; CI: Confidence interval;
The findings of this study were consistent with previ- MBR: Monthly biting rate; S: Simulium; s.l: sensu lato
ous studies conducted in Ghana [9] and Sudan [5], in
Acknowledgements
which the breeding sites of black flies were reduced due Thanks are extended to the local communities of the study sites in Galabat
to construction of dams. The chance of disease elimin- sub-focus for their cooperation during the collection of samples. Special
ation in the Galabat sub-focus increased when the upper thanks to Professor James Fox, Associate Professor of English, Ohio University
Zanesville, US, for reviewing and editing the manuscript.
north limit of the sub-focus became a lake.
The identified aquatic stages were revealed to be Authors’ contributions
anthropophilic species (S. damnosum s.l.) and two zoo- IMAZ, KH and DAB made substantial contributions to the conception and
the design of the study. IMAZ, AE, SGG, AKA, AA, HAS, DMA, OAS, OJO and
philic species (S. griseicolle, and S. adersi). They shared DAB did the field work. IMAZ, AE, SGG, AKA, AA, HAS, DMA, and DAB did the
same breeding sites, comprised of rocks and vegetation laboratory work. IMAZ and AE did the analysis and data interpretation. NA
in the Atbara River, but they differed in abundance and and DAB made contribution for survey facility and materials. IMAZ and AE
drafted the manuscript. IMAZ, AE, SGG, AKA, AA, HAS, DMA, OAS, OJO, DB,
distribution alongside the river. Most of S. damnosum NA and KH critically revised the manuscript; all authors read and approved
s.l. were found upstream of the dam complex (towards the final manuscript.
the Ethiopian border) where the speed of water was very
Funding
high and many rapids were found. S. griseicolle and S. Not applicable.
adersi predominated downstream of the dam complex
where the water current was low. This observation was Availability of data and materials
mentioned early in previous studies [17, 26, 27]. All data generated or analyzed during this study are included in thispublished article.
The presence of high numbers of aquatic stages of S.
damnosum s.l. at Balashora site, adjacent to the Ethiop- Ethics approval and consent to participate
ian border, may support the idea of considering the The study was approved by the community leaders, Gedarif state MOH, andthe Federal Ministry of Health, Sudan. Ethical approval for the study was
Galabat sub-focus in Sudan and the Metema sub-focus provided by the Federal Ministry of Health, Sudan as a part of the national
in Ethiopia as one transmission zone. This consideration onchocerciasis elimination/control program.
was supported previously by Raybould and White [26]
Consent for publication
who suggested control measures to be taken by the gov- Not applicable.
ernments of Sudan and Ethiopia.
The nearest Sudanese focus to the Galabat sub-focus Competing interests
The authors declare that they have no competing interests.
is more than 600 km at “Khor Yabus,” and the chance
for new infection or recrudescence will be low if the dis- Author details
1
ease is eliminated from Galabat. This is similar to the Onchocerciasis Control/Elimination Programme, National Programme for
Prevention of Blindness (NPPB), Federal Ministry of Health, Khartoum, Sudan.
isolation of the Abu-Hamed focus after Merowe Dam 2Department of Parasitology and Medical Entomology, Faculty of Medical
was built in 2009 [5]. Conscientious monitoring of Laboratory Sciences, University of Khartoum, Khartoum, Sudan. 3Department
breeding sites in front of the dam complex is imperative. of Immunology and Biotechnology, Tropical Medicine Research Institute,
National Center for Research, Khartoum, Sudan. 4Department of Medical
An agreement between Sudan and Ethiopia is required Entomology, Blue Nile National Institute for Communicable Diseases,
to eliminate the disease from the one transmission zone University of Gezira, Gezira, Sudan. 5Department of Medical Entomology,
in the area. National Public Health Laboratory, Federal Ministry of Health, Khartoum,
Sudan. 6Department of Epidemiology, Federal Ministry of Health, Khartoum,
Sudan. 7Department of Pure and Applied Zoology, Federal University of
Agriculture, Abeokuta, Nigeria. 8Department of Research and Development,
Conclusions Mission to Save the Helpless (MITOSATH), Jos, Nigeria.
9Parasitology
Department, Noguchi Memorial Institute for Medical Research, University of
Construction of the Upper Atbara and Setit Dam complex Ghana, Accra, Ghana. 10The Carter Center, Khartoum, Sudan. 11National
and its artificial lake had changed the physical, biological, Programme for Prevention of Blindness (NPPB), Federal Ministry of Health,
and socio-economic environment of the affected breeding Khartoum, Sudan.
sites in the Galabat sub-focus. The dam complex has Received: 11 December 2017 Accepted: 20 May 2019
produced a positive effect by reducing the breeding sites
of black flies in the area. Agreement on an action plan for
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