J Arthropod-Borne Dis, December 2019, 13(4): 420–425 KE Benallal et al.: First Detection of … 420 http://jad.tums.ac.ir Published Online: December 31, 2019 Case Report First Detection of Aedes (Stegomyia) albopictus (Diptera: Culicidae) in Algiers, the Capital City of Algeria *Kamel Eddine Benallal, Rafik Garni, Lazhari Bouiba, Zoubir Harrat Laboratoire d’Eco-épidémiologie Parasitaire et Génétique des Populations, Institut Pasteur d’Algérie, Route Petit Staouéli, Dely Ibrahim, Alger, Algérie (Received 13 Mar 2017; accepted 13 Oct 2019) Abstract Background: Based on the reporting of the presence of stripped mosquitoes by a citizen in the Algiers residential neighborhood of Bir-Khadem, where residents experienced huge daytime mosquito nuisance an entomological inves- tigation was carried out in July 2016. Methods: Ovitraps and BG sentinel traps baited with Lure were used during three consecutive days to collect adult mosquitoes. Eighteen residential houses of the Bir-Khadem neighborhood were also inspected to search larvae breed- ing sites such as water fountains, baskets and flowerpots. Results: A total of 57 Aedes albopictus specimens were collected in five villas, consisting of 21 eggs, 20 larvae and 16 adults. Conclusion: This is the first record of this invasive species in Algiers. Keywords: Aedes albopictus, Mosquitoes, Arbovirus, Algiers, Algeria Introduction Aedes albopictus is currently considered the most invasive mosquito species (1) as its rapid adaptation to a large variety of environments in both tropical and temperate areas has al- lowed its spread throughout the world (2). In- deed, Ae. albopictus larvae can breed in dif- ferent container forms (3). As early as 1968, Ae. albopictus was reported as the most com- mon and widespread mosquito in Southeast Asia (4). In 1979, this mosquito was reported in Albania (5) then in several countries in Eu- rope, around the Mediterranean basin and in Morocco (6, 7). Doubtlessly, the worldwide dis- persion of Ae. albopictus is mainly caused ei- ther by trade in used tires or lucky bamboo be- tween the continents and by travelers and cars within land (8, 9). Beside its huge nuisance, Ae. albopictus capacity to spread could engender a serious threat for the public health since it is compe- tent to transmit several viruses (10). This mos- quito has been responsible for the large out- break of Chikungunya in La Réunion Island and focal transmission of Dengue and Chikungu- nya in Europe (11–13). Since then because of its ability to adapt to different environments, this mosquito species is under scrutiny by many health services. It has also been shown to be competent for Zika virus (10, 14) but its role in the current Zika epidemics needs further in- vestigation. Aedes albopictus is also known as a vector for West Nile virus (15, 16), Dirofi- laria immitis and D. repens (17, 18). In Al- geria, it was reported on three occurrences (19-21), but never in Algiers, the capital city of Algeria. In July 2016, a citizen contacted our la- boratory to complain from strange mosquitoes that caused painful bites and huge daytime nui- sance. The herein entomological survey led to the identification of Ae. albopictus in the district of Bir-Khadem and assessed its spread in the district. *Corresponding author: Dr Kamel Eddine Benallal, E-mail: benallalkamel4@yahoo.fr http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 420–425 KE Benallal et al.: First Detection of … 421 http://jad.tums.ac.ir Published Online: December 31, 2019 Materials and Methods Bir-Khadem is a locality of Algiers (alti- tude 84m, 36.716460° N, 3.042561° E), pop- ulation number 77. 749 persons located about 6km from the commercial port and 16km off the international airport. In Algiers, Mediter- ranean climate occurs with a mean 686mm rainfall per year and a mean temperature of 23 °C. A citizen living in a residential neighbor- hood brought to our laboratory some mosqui- to specimens collected in his house. These mos- quitoes bite during daytime and made a huge nuisance, which was suggestive of Ae. albopic- tus. Following this, sampling procedures for detecting invasive mosquitoes were implement- ed in that neighborhood. Two Biogents-Sentinel™ trap (BGS) (Bio- gents AG, Regensburg, Germany) baited with BG-Lure (BGL) a mosquito attractive were run outside in the gardens (first at the house of the complainer and the second at the house of the Asian persons) for three consecutive days to collect adult mosquitoes. A total of 18 resi- dential houses of the Bir-Khadem neighbor- hood were also inspected in order to search possible larval breeding sites such as water fountains, baskets and flowerpots plates. Ovit- raps consisting of black plastic container filled with 400ml of water and leaves provided with a 20× 20× 5cm of polyester piece as a substrate for Aedes spp. mosquito oviposition device were placed under trees and in shaded areas (11). The collected adult and larvae specimens were morphologically identified (22). A survey with local citizens (18 house- holds) about the first appearance of this mos- quito in the area was carried out mainly was around: i) the period of biting and activity of this species (daytime or night), ii) what is new in the neighborhood (the installation of new people, a new commercial activity especially that of used tires or the sale of exotic plants), iii) the notion of travel in countries endemic to Ae. albopictus. All these questions were asked in order to find an explanation how this mos- quito has came to this area since it was reported established only in Oran which is distanced about 500km from Algiers (21). Results The eight mosquitoes (two males and six females) collected by the citizen belonged to Aedes genus showed black and white stripes showed black and white stripes on their legs and a medio-dorsal white stripe on the thorax characteristic of Ae. albopictus. Out of the 18 residential houses prospected 4 were positives with Ae. albopictus in association with Culex pipiens and Culiseta longiareolata around the Asian foreign villas (Table 1, Fig. 1). A total of fifty-seven adults of Ae. albopictus (male and female) were identified either collected at adult stages or emerged from larvae and nymphs. The survey carried out with local citizens revealed that this species bites in daytimes and had appeared one month before in June and coincided with the installation of Asian persons who work for a building company in Algiers. They had not reported new com- mercial activities (tires or plants) since it was a residential quarter. Concerning travelling notion no one had been in an endemic area of Ae. albopictus. Table 1. Location and stage of Aedes albopictus collected during the survey House Specimen numbers Adultes Larvae Eggs P1 P2 P3 P4 Total 13 11 / / 24 15 / / 5 20 7 / 6 / 13 P1: villa where first specimens were collected, P2: foreign’s villa, P3: second positive villa, P4: third positive villa http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 420–425 KE Benallal et al.: First Detection of … 422 http://jad.tums.ac.ir Published Online: December 31, 2019 Fig. 1. Location of Aedes albopictus captures at different development stages Discussion An entomological survey was implement- ed in a residential neighborhood of Bir-Khadem in order to identify the mosquito species im- plicated in the source of nuisance. As suspected, several specimens of Ae. albopictus were found. Residential houses with garden, swimming pool, vegetation, trees and animals provide suit- able environmental conditions for this species to reproduce. In addition, the stability of good climate conditions during June till August 2016 (mean temperature 25 °C) has allowed Ae. albopictus to reproduce and colonize easily this area. The occurrence of this species in this lo- cality with mean annual precipitation of 686 mm is of great interest since over most of its range is associated with very heavy rainfall (23). BG-Sentinel traps and ovitraps allow the collection of few specimens only. This sug- gests that Ae. albopictus population is still at low level despite favorable environmental con- ditions or at the beginning of its introduction. Besides, the questionnaire survey carried out with the citizens revealed that this mosquito had appeared since June 2016. One might wonder whether the source of Ae. albopictus could be some eggs carried in the plants that they brought from their country and cultivated in their garden for their own consummation since no commercial activity nor tire manufactory are registered in this area. Aedes albopictus is well established all around the Mediterranean basin and risk-map- ping modeling showed that Northern Algeria is suitable for its installation (24). Since the report of dengue and Chikungunya in Europe (25, 26) and several cases of West Nile in Al- geria (27, 28), the Algerian Government has established an arbovirus surveillance system according to the International Health Regula- tion. Unfortunately, the surveillance system set- up has not allowed the early detection of Ae. al- bopictus introduction into Algeria but thanks to the vigilance of inhabitants who reported these mosquitoes which proves that implication of citizens remains the most important way to re- port and monitor the establishment of invasive mosquitoes (11). Even if insecticide (Allethrin) spraying was performed by Algiers Board of http://jad.tums.ac.ir/ J Arthropod-Borne Dis, December 2019, 13(4): 420–425 KE Benallal et al.: First Detection of … 423 http://jad.tums.ac.ir Published Online: December 31, 2019 Health to eliminate adults before possible es- tablishment, a continuous surveillance with ovitraps and BG-sentinel traps is highly rec- ommended to monitor its extension area since Ae. albopictus is known to skip oviposition and to release its eggs in several breeding sites (29). A good communication campaign in radio and television should be also planned as it is a new mosquito species with new behavior in order to explain to citizens how avoiding the development of this species in their garden and how to limit its propagation by simple gestures like covering the water barrels, emptying the flowerpot plates, removing unnecessary uten- sils from the gardens and the surrounding ar- eas that may contain water and help the pullu- lation of these mosquitoes. Such measures need to be planned before for limiting Ae. albopic- tus propagation to other areas and to avoid the massive using of insecticides for vector con- trol which could favor the appearance of re- sistance with time. Conclusion The fourth record of A. albopictus in Al- geria suggests that the surveillance system ef- ficiency must be improved by sensitizing and implicating population awareness for this mos- quito species in time. Furthermore, involvement of Ae. albopictus in the transmission of Den- gue, Chikungunya, and Zika viruses from vi- remic persons highlights the importance of monitoring this invasive species to assess the health risk. Further studies are recommended to determine the origin of the specimens col- lected in Algiers, and to investigate the ecolo- gy and sensitivity to insecticides of this species in case it establishes in Algiers for planning adapted and efficient control measures. Acknowledgements We would like to thank all the inhabitants of the residential area especially Mr Karim Ou- dina for their help during entomological inves- tigations, and C Bourgouin (GFMI, Institut Pas- teur-Paris) for useful comments. The authors declare that there is no con- flict of interests. References 1. Enserink M (2008) A mosquito goes glob- al. Science. 320: 864–866. 2. Gould EA, Higgs S (2009) Impact of climate change and other factors on emerging ar- bovirus diseases. Trans R Soc Trop Med Hyg. 103: 109–121. 3. Hawley WA, Reiter P, Copeland RS, Pumpuni CB, Craig GB JR (1987) Ae- des albopictus in North America: prob- able introduction in used tires from north- ern Asia. Science. 236: 1114–1116. 4. Huang YM (1968) Neotype designation for Aedes (Stegomyia) albopictus (Skuse) (Diptera: Culicidae). Proc Ent Soc Wash. 70: 297–302. 5. Adhami J, Reiter P (1998) Introduction and establishment of Aedes (Stegomyia) al- bopictus Skuse (Diptera: Culicidae) in Albania. J Am Mosq Control Assoc. 14: 340–343. 6. Technical report: Development of Aedes albopictus risk maps (2009) ECDC, Stockholm. Available at: http://ecdc.europa.eu/en/healthtopics/v ectors/vector- maps/Pages/VBORNET_maps.aspx. 7. Bennouna A, Balenghien T, Rhaffouli H, Schaffner F, Garros C, Gardès L, Lhor Y, Hammoumi S, Chlyeh G, Fassi-Fihri O (2016) First record of Stegomyia al- bopicta (= Aedes albopictus) in Morocco: a major threat to public health in North Africa? Med Vet Entomol. 31(1): 102– 106. 8. Pluskota B, Storch V, Braunbeck T, Beck M, Becker N (2008) First record of Stegomyia albopicta (Skuse) (Diptera: http://jad.tums.ac.ir/ https://www.google.dz/url?sa=t&rct=j&q=&esrc=s&source=web&cd=2&cad=rja&uact=8&ved=0ahUKEwia3snixvnKAhWGfRoKHRB4AIEQjBAIJjAB&url=http%3A%2F%2Ftrstmh.oxfordjournals.org%2Fcontent%2Fby%2Fyear&usg=AFQjCNFHjgiHcZQS7TtyrR-N_CWOI-jvag&sig2=9KA9xRhjhlhRJh4yV6Lu4Q https://www.google.dz/url?sa=t&rct=j&q=&esrc=s&source=web&cd=2&cad=rja&uact=8&ved=0ahUKEwia3snixvnKAhWGfRoKHRB4AIEQjBAIJjAB&url=http%3A%2F%2Ftrstmh.oxfordjournals.org%2Fcontent%2Fby%2Fyear&usg=AFQjCNFHjgiHcZQS7TtyrR-N_CWOI-jvag&sig2=9KA9xRhjhlhRJh4yV6Lu4Q http://ecdc.europa.eu/en/healthtopics/vectors/vector-maps/Pages/VBORNET_maps.aspx http://ecdc.europa.eu/en/healthtopics/vectors/vector-maps/Pages/VBORNET_maps.aspx http://ecdc.europa.eu/en/healthtopics/vectors/vector-maps/Pages/VBORNET_maps.aspx https://www.ncbi.nlm.nih.gov/pubmed/?term=Bennouna%20A%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=Balenghien%20T%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=El%20Rhaffouli%20H%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=El%20Rhaffouli%20H%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=Schaffner%20F%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=Garros%20C%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=Gard%C3%A8s%20L%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=Lhor%20Y%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=Hammoumi%20S%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=Chlyeh%20G%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=Fassi%20Fihri%20O%5BAuthor%5D&cauthor=true&cauthor_uid=27775162 https://www.ncbi.nlm.nih.gov/pubmed/?term=benouna+aedes+albopictus+morocco J Arthropod-Borne Dis, December 2019, 13(4): 420–425 KE Benallal et al.: First Detection of … 424 http://jad.tums.ac.ir Published Online: December 31, 2019 Culicidae) in Germany. Euro Mosq Bull. 26: 1–5. 9. Müller GC, Tsabari O, Traore MM, Traore SF, Doumbia S, Kravchenko VD, Jun- nila A, Beier JC (2016) First record of Aedes albopictus in inland Africa along the River Niger in Bamako and Mopti, Mali. Acta Trop. 162: 245–247. 10. Glida G, Caron M, Mombo IM, Nkoghe D, Ondo SM, Davy J, Fontenille D, Pau- py C, Leroy EM (2014) Zika Virus in Gabon (Central Africa) –2007: A New Threat from Aedes albopictus? PLoS Negl Trop Dis. 8(2): e2681. 11. Barceló C, Bengoa M, Monerris M, Mo- lina R, Delacour-Estrella S, Lucientes J, Miranda MA (2015) First record of Aedes albopictus (Skuse, 1894) (Diptera: Cu- licidae) from Ibiza (Balearic Islands; Spain). J Euro Mosq Control Assoc. 33: 1–4. 12. Franke F, Septfons A, Leparc-Goffart I, Giron S, Guinard A, Burdet S (2016) Surveillance du chikungunya, de la den- gue et des infections à virus Zika en France métropolitaine 2017. Bull Epidé- miol Hebd. 2017(12): 222–231 13. Giovanni R (2018) Chikungunya is back in Italy: 2007–2017. J Travel Med. 25: 1–4. 14. Di Luca M, Severini F, Toma L, Bocco- lini D, Romi R, Remoli ME, Sabbatucci M, Rizzo C, Venturi G, Rezza G, For- tuna C (2016) Experimental studies of susceptibility of Italian Aedes albopic- tus to Zika virus. Euro Surveill. 21(18). 15. Medlock JM, Hansford KM,Schaffner F, Versteirt V, Hendrickx G, Zeller H, Bortel WV (2012) A Review of the In- vasive Mosquitoes in Europe: Ecology, Public Health Risks, and Control Options Vector-Born Zoo Diseas. 12(6): 435–447. 16. Fortuna C, Remoli ME, Severini F, Di Luca M, Toma L, Fois F, Bucci P, Boccolini D, Romi R, Ciufolini MG (2015) Eval- uation of vector competence for West Nile virusin Italian Stegomyia albopicta (=Aedes albopictus) mosquitoes. Med Vet Entomol. 29: 430–433. 17. Cancrini G, Frangipane Di Regalbono AF, Ricci I, Tessarin C, Gabrielli S, Pietro- belli M (2003) Aedes albopictus is a natural vector of Dirofilaria immitis in Italy. Vet Parasitol. 118: 195–202. 18. Cancrini G, Scaramozzino P, Gabrielli S, Di Paolo M, Toma L, Romi R (2007) Aedes albopictus and Culex pipiens im- plicated as natural vectors of Dirofi- laria repens in central Italy. J Med En- tomol. 44(6): 1064–1066. 19. Izri A, Bitam I, Charrel RN (2011) First entomological documentation of Aedes (Stegomyia) albopictus (Skuse, 1894) in Algeria. Clin Microbiol Infect. 17: 7. 20. Lafri I, Bitam I, Beneldjouzi A, Ben Mah- di MH (2014) An inventory of mosque- toes (Diptera: Culicidae) in Algeria. Bull Soc Zool Fr. 139(1–4): 255–261. 21. Benallal KE, Allal-Ikhlef A, Benhamou- da K, Schaffner F, Harra Z (2016) First report of Aedes (Stegomyia) albopictus (Diptera: Culicidae) in Oran, West of Algeria. Acta Trop. 164: 411–413. 22. Schaffner F, Angel G, Geoffroy B, Her- vy JP, Rhaiem A, Brunhes J (2001) The Mosquitoes of Europe /Les moustiques d'Europe. Logiciel d'identification et d'enseignement (CD-Rom), Montpel- lier, France, IRD Editions and EID Mé- diterranée. 23. Qutubuddin M (1960) The mosquito fau- na of Kohat-Hangu valley, West Paki- stan. Mosquito News. 20(40): 355–361. 24. Kraemer MUG, Sinka ME, Duda KA, Mylne AQN, Shearer FM, Barker CM, Moore CG, Carvalho RG, Coelho GE, Van Bortel W, Hendrickx G, Schaffner F, Elyazar IR, Teng HJ, Brady OJ, Mes- sina JP, Pigott DM, Scott TW, Smith DL, Wint GR, Golding N, Hay SI (2015) The global distribution of the arbovirus vectors Aedes aegypti and Ae. Albopictus. Elife. 4: e08347. http://jad.tums.ac.ir/ https://www.ncbi.nlm.nih.gov/pubmed/?term=Di%20Luca%20M%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Severini%20F%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Toma%20L%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Toma%20L%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Boccolini%20D%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Romi%20R%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Remoli%20ME%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Remoli%20ME%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Sabbatucci%20M%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Rizzo%20C%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Venturi%20G%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Rezza%20G%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Rezza%20G%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Fortuna%20C%5BAuthor%5D&cauthor=true&cauthor_uid=27171034 https://www.ncbi.nlm.nih.gov/pubmed/?term=Cancrini%20G%5BAuthor%5D&cauthor=true&cauthor_uid=18047207 https://www.ncbi.nlm.nih.gov/pubmed/?term=Scaramozzino%20P%5BAuthor%5D&cauthor=true&cauthor_uid=18047207 https://www.ncbi.nlm.nih.gov/pubmed/?term=Gabrielli%20S%5BAuthor%5D&cauthor=true&cauthor_uid=18047207 https://www.ncbi.nlm.nih.gov/pubmed/?term=Di%20Paolo%20M%5BAuthor%5D&cauthor=true&cauthor_uid=18047207 https://www.ncbi.nlm.nih.gov/pubmed/?term=Toma%20L%5BAuthor%5D&cauthor=true&cauthor_uid=18047207 https://www.ncbi.nlm.nih.gov/pubmed/?term=Romi%20R%5BAuthor%5D&cauthor=true&cauthor_uid=18047207 https://www.ncbi.nlm.nih.gov/pubmed/18047207 https://www.ncbi.nlm.nih.gov/pubmed/18047207 J Arthropod-Borne Dis, December 2019, 13(4): 420–425 KE Benallal et al.: First Detection of … 425 http://jad.tums.ac.ir Published Online: December 31, 2019 25. Rezza G, Nicoletti L, Angelini R, Romi R, Finarelli AC, Panning M, Cordioli P, Fortuna C, Boros S, Magurano F, Silvi G, Angelini P, Dottori M, Ciufolini MG, Majori GC, Cassone A; CHIKV study group (2007) Infec-tion with CHIKV in Italy: an outbreak in a tem- perate region. The Lancet. 370 (9602): 1840–1846. 26. La Ruche G, Dejour-Salamanca D, De- bruyne M, Leparc-Goffart I, Ledrans M, Grandadam M, Brichler S, Souares Y, Denoyel GA, Poveda JD, Gastellu-Et- chegorry M (2010) Surveillance par les laboratoires des cas de dengue et de chi- kungunya importés en France métropo- litaine 2008–2009. BEH. 31–32: 325–329. 27. Santé publique France, Institut de Veille Sanitaire (2012) Bulletin épidémiolo- gique hebdomadaire. 10–16 October 2012. p. 369. 28. Lafri I, Hachid A, Bitam I (2019) West Nile virus in Algeria: a comprehensive over- view. New Microbe and New Infect. 27: 9–13. 29. Davis TJ, Kaufman PE, Hogsette JA, Kline DL (2015) The effects of larval habitat quality on Aedes albopictus skip ovipo- sition. J Am Mosq Control Assoc. 31 (4): 321–328. http://jad.tums.ac.ir/