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Five years following first detection of Anopheles stephensi (Diptera: Culicidae) in Djibouti, Horn of Africa: populations established—malaria emerging

Abstract

The Asian malaria mosquito, Anopheles stephensi, is a well-known and important vector of Plasmodium falciparum and P. vivax. Until 2013, its geographical distribution was confined to central and southern Asia including the Arabian Peninsula. In the Horn of Africa (HoA) Region, An. stephensi was first recorded from Djibouti in 2012, when it was linked geographically and temporally with an unusual outbreak of urban P. falciparum malaria. In 2016, An. stephensi was detected in the neighbouring Somali Region of Ethiopia. In order to determine whether An. stephensi populations have become established in Djibouti and contributed to the unusual rise in local malaria cases there, we carried out continuous vector surveillance from January 2013 to December 2017, investigated seasonal changes in An. stephensi population densities and bionomics, analysed available literature describing malaria in Djibouti since 2013, and investigated whether An. stephensi may have contributed to local malaria transmission by detecting circumsporozoite antigen of P. falciparum and P. vivax in female anophelines. From 2013 to 2016, seasonal activity of An. stephensi in urban Djibouti City primarily occurred during the colder, wetter season between September and May, with either no or rare trap catches from June to August. Unlike past years, this species was detected year-round, including the extremely hot summer months of June to August 2017. This change in seasonal occurrence may indicate that An. stephensi populations are adapting to their new environment in sub-Saharan Africa, facilitating their spread within Djibouti City. Among the 96 female An. stephensi investigated for malaria infectivity, three (3.1%) were positive for P. falciparum circumsporozoite antigen, including one P. falciparum/P. vivax VK 210 double infection. Subsequent to the unusual resurgence of local malaria in 2013, with 1684 confirmed cased reported for that year, malaria case numbers increased continuously, peaking at 14,810 in 2017. Prior to 2016, only P. falciparum malaria cases had been reported, but in 2016, autochthonously acquired P. vivax malaria cases occurred for the first time at a rate of 16.7% among all malaria cases recorded that year. This number increased to 36.7% in 2017. Our data indicate that the dynamics of malaria species in Djibouti is currently changing rapidly, and that An. stephensi can be involved in the transmission of both P. falciparum and P. vivax, simultaneously. Considering the extremely high potential impact of urban malaria on public health, the timely deployment of optimal multinational vector surveillance and control programs against An. stephensi is strongly recommended, not only for the HoA Region, but for the entire African continent.

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References

  1. Abduselam N, Zeynudin A, Berens-Riha N, Seyoum D, Pritsch M, Tibebu H, Eba K, Hoelscher M, Wieser A, Yewhalaw D (2016) Similar trends of susceptibility in Anopheles arabiensis and Anopheles pharoensis to Plasmodium vivax infection in Ethiopia. Parasit Vectors 9:552

  2. Armed Forces Health Surveillance Branch (AFHSB) (2015) Update: malaria, U.S. Armed Forces, 2014. MSMR. 22(1):2–6

  3. Armed Forces Health Surveillance Branch (AFHSB) (2016) Update: malaria, U.S. Armed Forces, 2015. MSMR. 23(1):2–6

  4. Armed Forces Health Surveillance Branch (AFHSB) (2017) Update: malaria, U.S. Armed Forces, 2016. MSMR 24(1):2–7

  5. Armed Forces Health Surveillance Branch (AFHSB) (2018) Update: malaria, U.S. Armed Forces, 2017. MSMR. 25(2):2–7

  6. Armed Forces Health Surveillance Center (AFHSC) (2012) Update: malaria, U.S. Armed Forces, 2011. MSMR. 19(1):2–6

  7. Armed Forces Health Surveillance Center (AFHSC) (2013) Update: malaria, U.S. Armed Forces, 2012. MSMR. 20(1):2–5

  8. Armed Forces Health Surveillance Center (AFHSC) (2014) Update: malaria, U.S. Armed Forces, 2013. MSMR. 21(1):2–7

  9. Asmare Y, Hill SR, Hopkins RJ, Tekie H, Ignell R (2017) The role of grass volatiles on oviposition site selection by Anopheles arabiensis and Anopheles coluzzii. Malar J 16:65

  10. Bangs M, Rusmiarto S, Gionar YR, Chan AST, Dave K, Ryan JR (2002) Evaluation of a dipstick malaria sporozoite panel assay for detection of naturally infected mosquitoes. J Med Entomol 39:324–330

  11. Carter TE, Yared S, Gebresilassie A, Bonnell V, Damodaran L, Lopez K, Ibrahim M, Mohammed S, Janies D (2018) First detection of Anopheles stephensi Liston, 1901 (Diptera: Culicidae) in Ethiopia using molecular and morphological approaches. Acta Trop 188:180–186. https://doi.org/10.1016/j.actatropica.2018.09.001. [Epub ahead of print]

  12. Das BP, Rajagopal R, Akiyama J (1990) Pictorial key to the species of Indian anopheline mosquitoes. Zoology 2:131–162

  13. Daygena TY, Massebo F, Lindtjørn B (2017) Variation in species composition and infection rates of Anopheles mosquitoes at different altitudinal transects, and the risk of malaria in the highland of Dirashe Woreda, South Ethiopia. Parasit Vectors 10:343

  14. de Pécoulas PE, Tahar R, Quatas T, Mazabraud A, Basco LK (1998) Sequence variations in the Plasmodium vivax dihydrofolate reductase-thymidylate synthase gene and their relationship with pyrimethamine resistance. Mol Biochem Parasitol 92:265–273

  15. Dharmasiri AGG, Perera AY, Harishchandra J, Herath H, Aravindan K, Jayasooriya HTR, Ranawaka GR, Hewavitharane M (2017) First record of Anopheles stephensi in Sri Lanka: a potential challenge for prevention of malaria reintroduction. Malar J 16:326

  16. Dida GO, Anyona DN, Abuom PO, Akoko D, Adoka AO, Matano A-S, Owuor PO, Ouma C (2018) 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 7(1):2

  17. Faulde MK, Ahmed AA (2010) Haematophageous vector monitoring in Djibouti City from 2008 to 2009: first records of Culex pipiens ssp. torridus (IGLISCH), and Anopheles sergentii (Theobald). J Egypt Soc Parasitol 40:281–294

  18. Faulde MK, Spiesberger M, Abbas B (2012) Sentinel-site-enhanced near-real time surveillance documenting West Nile virus circulation in two Culex mosquito species indicating different transmission characteristics, Djibouti City, Djibouti. J Egypt Soc Parasitol 42:461–474

  19. Faulde MK, Rueda LM, Khaireh BA (2014) First record of the Asian malaria vector Anopheles stephensi and its possible role in the resurgence of malaria in Djibouti, Horn of Africa. Acta Trop 139:39–43

  20. Gillies MT, Coetzee M (1987) A supplement to the Anophelinae of Africa south of the Sahara (Afrotropical Region). South African Institute for Medical Research, Johannesburg, South Africa, pp 1–147

  21. Glick JI (1992) Illustrated key to the female Anopheles of southwestern Asia and Egypt (Diptera: Culicidae). Mosq Syst 24:125–153

  22. Howes RE, Reiner RC Jr, Battle KE, Longbottom J, Mappin B, Ordanovich D, Tatem AJ, Drakeley C, Gething PW, Zimmermann PA, Smith DL, Hay SI (2015) Plasmodium vivax transmission in Africa. PLoS Negl Trop Dis 9(11):e0004222

  23. Hume JCC, Tunnicliff M, Ranford-Cartwright LC, Day KP (2007) Susceptibility of Anopheles gambiae and Anopheles stephensi to tropical isolates of Plasmodium falciparum. Malar J 6:139

  24. Khaireh BA, Briolant S, Pascual A, Mokrane M, Machault V, Travaillé C, Khaireh MA, Farah IH, Ali HM, Abdi A-IA, Ayeh SN, Darar HY, Ollivier L, Waiss MK, Bogreau H, Rogier C, Pradines B (2012) Plasmodium vivax and Plasmodium falciparum infections in the Republic of Djibouti: evaluation of their prevalence and potential determinants. Malar J 11:e395

  25. Khaireh BA, Assefa A, Guessod HH, Basco LK, Khaireh MA, Pascual A, Briolant S, Bouh SM, Farah IH, Ali HM, Abdi A-IA, Aden MO, Abdillahi Z, Ayeh SN, Darar HY, Koeck J-L, Rogier C, Pradines B, Bogreau H (2013) Population genetics analysis during elimination process of Plasmodium falciparum in Djibouti. Malar J 12:201

  26. Nina PB, Mohanty AK, Ballav S, Vernekar S, Bhinge S, D’souza M, Walke J, Manoharan SK, Mascarenhas A, Gomes E, Chery L, Valecha N, Kumar A, Rathod PK (2017) Susceptibility of wild and colonized Anopheles stephensi to Plasmodium vivax infection. Malar J 16:284

  27. Ollivier L, Nevin RL, Darar HY, Bougere J, Saleh M, Gidenne S, Maslin J, Anders D, Decam C, Todesco A, Khaireh BA, Ahmed AA (2011) Malaria in the Republic of Djibouti, 1998-2009. Am J Trop Med Hyg 85:554–559

  28. Rodier GR, Parra JP, Kamil M, Chakib SO, Cope SE (1995) Recurrence and emergence of infectious diseases in Djibouti city. Bull World Health Organ 73:755–759

  29. Rogier C, Pradines B, Bogreau H, Koeck J-L, Kamil M-A, Mercereau-Puijalon O (2005) Malaria epidemic and drug resistance, Djibouti. Emerg Infect Dis 11:317–321

  30. United Nations (2013) Djibouti: Appel global – Revue à mi-parcours 2013. [accessed 2018 July 02]. Available from https://www.humanitarianresponse.info/fr/programme-cycle/space/document/revue-%C3%A0-mi-parcours-de-lappel-global-pour-djibouti-2013

  31. Walter Reed Biosystematics Units (WRBU) (2012) Vector identification resources. [accessed 2012 Oct 25]. Available from http://www.wrbu.org/keys/CP_AN_A/Anopheles_W_Palearc_CENTCOM_A.html

  32. WHO (2012) World malaria report 2011. Available from http://www.who.int/malaria/publications/world_malaria_report_2012/wmr2012_full_report.pdf. Accessed 21 Aug 2018

  33. WHO (2013) World malaria report 2012. Available from http://www.who.int/malaria/publications/world_malaria_report_2013/report/en/. Accessed 21 Aug 2018

  34. WHO (2014a) A global brief on vector-borne diseases Available from http://apps.who.int/iris/bitstream/10665/111008/1/WHO_DCO_WHD_2014.1_eng.pdf. Accessed 07 Aug 2018

  35. WHO (2014b) World malaria report 2013. Available from http://www.who.int/malaria/publications/world_malaria_report_2014/report/en/. Accessed 21 Aug 2018

  36. WHO (2015) World malaria report 2014. Available from http://www.who.int/malaria/publications/world-malaria-report-2015/report/en/. Accessed 21 Aug 2018

  37. WHO (2016) World malaria report 2015. Available from http://www.who.int/malaria/publications/world-malaria-report-2016/report/en/. Accessed 21 Aug 2018

  38. WHO (2017a) Global vector control response 2017–2030. Available from http://www.who.int/malaria/areas/vector_control/Draft-WHO-GVCR-2017-2030.pdf. Accessed 07 Aug 2018

  39. WHO (2017b) World malaria report 2016. Available from http://www.who.int/malaria/publications/world-malaria-report-2017/report/en/. Accessed 21 Aug 2018

  40. Wilson ML, Krogstad DJ, Arinaitwe E, Arevalo-Herrera M, Chery L, Ferreira MU, Ndiaye D, Mathanga DP, Eapen A (2015) Urban malaria: understanding its epidemiology, ecology, and transmission across seven diverse ICEMR network sites. Am. J. Trop. Med. Hyg. 93(Suppl 3):110–123

  41. World Factbook (2018) Djibouti. World Factbook, CIA, USA, June 07, 2018. [accessed 2018 June 22]. Available from https://www.cia.gov/library/publications/the-world-factbook/geos/dj.html

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Acknowledgements

The authors thank Ms. Anke Crecelius and Ms. Munar-Herrmann for laboratory support. Thanks are also given to the military personnel involved who assisted in data collection. Dr. Richard G. Robbins, Walter Reed Biosystematics Unit, Department of Entomology, Smithsonian Institution, Washington, DC, helpfully reviewed and commented on an the earlier version of our manuscript. This publication represents the thesis of Mr. Marco Seyfarth.

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Correspondence to Michael K. Faulde.

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Seyfarth, M., Khaireh, B.A., Abdi, A.A. et al. Five years following first detection of Anopheles stephensi (Diptera: Culicidae) in Djibouti, Horn of Africa: populations established—malaria emerging. Parasitol Res 118, 725–732 (2019). https://doi.org/10.1007/s00436-019-06213-0

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Keywords

  • Anopheles stephensi
  • Invasive species
  • Malaria
  • Outbreak
  • Plasmodium falciparum
  • Plasmodium vivax