Open Access

First report on human-biting Culex pipiens in Sweden

Parasites & Vectors20169:632

DOI: 10.1186/s13071-016-1925-3

Received: 15 November 2016

Accepted: 1 December 2016

Published: 7 December 2016

Abstract

Culex mosquitoes are vectors of several bird-hosted arboviruses that cause outbreaks in Europe, such as Sindbis virus and West Nile virus. Recently, the human-biting form of Culex pipiens, Cx. pipiens biotype molestus, was found causing big nuisance in a housing cooperative in Gothenburg in southern Sweden, confirmed by molecular identification. This is the first report of human-biting Culex in Scandinavia, signalling increased risk of arbovirus infection in northern Europe.

Keywords

Vector-borne infections West Nile virus Zoonoses Mosquito vector Arbovirus Sindbis virus

Letter to the Editor

Mosquitoes of the genus Culex are the vectors of bird-hosted arboviruses that occasionally cause disease in humans, such as Sindbis virus (SINV) (Alphavirus) West Nile virus (WNV) and Usutu virus (USUV) (Flavivirus), all circulating in Europe. Seven potential vector species are recognised within the genus Culex in Europe, most of which show a preference for biting birds (ornithophilic). One of the species, the northern house mosquito Cx. pipiens, has been described as having two separate biotypes: Cx. pipiens biotype pipiens and Cx. pipiens biotype molestus, of which the latter fulfils certain criteria that separates it from the other: it does not hibernate in winter (homodynamic), it utilizes underground larval habitat (hypogeous), it can mate in confined spaces (stenogamous), it can lay its first egg batch without a blood meal (autogenous), and it feeds on humans (mammophilic). Culex pipiens biotype molestus has been reported from many central and southern European countries but never from Scandinavia [14]. Hybridisation of the two biotypes is quite common in the Mediterranean area, while hybrids are less commonly found in central Europe [3, 4]. Culex pipiens biotype molestus and potential hybrids are of high concern since they have the potential to serve as bridge vectors of these arboviruses from birds to humans, as they possess the vector competence of Cx. pipiens biotype pipiens [5] but an opportunistic feeding behaviour [6].

The last countrywide mosquito survey recognised three Culex species as endemic to Sweden: the ornithophilic species Cx. torrentium, Cx. pipiens biotype pipiens and Cx. territans that primarily feeds on ectothermic hosts [7]. Recently, an encounter with Cx. modestus that commonly bite man in central European countries has also been reported from southern Sweden [8].

In August 2016, one of the authors visited a private housing cooperative situated approximately 4 km south west of central Gothenburg, Sweden, that had experienced problems with mosquitoes biting tenants indoors. The housing cooperative is a property of approximately 4.5 ha with seven blocks of three-storey buildings. It is located in a residential area with similar buildings, intermixed with smaller park areas with deciduous bushes and trees. An online survey among the tenants showed that nearly 100 households (roughly a third of all flats in the cooperative), distributed throughout all the buildings and on all three floors of the cooperative, had problems with mosquitoes biting indoors. The earliest complaint of indoor biting was in winter/spring 2015, and since then the problem seems to have gradually increased, showing peaks in summer and autumn but also occurring during wintertime. The mosquitoes were reported to enter through open windows and balcony doors, as well as through the ventilation system on all three floors, and to be aggressive biters on humans during evening and night-time. Eleven female Culex mosquitoes were caught as they tried to bite humans, and Culex larvae were sampled in a catch basin just outside one of the affected buildings.

The eleven adult Culex females caught indoors and ten larvae from the outside catch basin were used for DNA extraction and molecular species identification. Since Cx. torrentium is the most common Culex species in Sweden, a first assay for separating Cx. torrentium and Cx. pipiens (s.l.) was run [9], identifying all 11 adults and ten larvae as Cx. pipiens (s.l.). The DNA was then amplified in a second PCR designed to distinguish between Cx. pipiens biotype pipiens and Cx. pipiens biotype molestus [10], resulting in identification of all 11 adults as Cx. pipiens biotype molestus (Fig. 1), and the ten larvae as Cx. pipiens biotype pipiens.
Fig. 1

Electrophoresis gel confirming the presence of Cx. pipiens biotype molestus in Sweden. PCR products from a diagnostic assay separating Cx. pipiens biotype pipiens and Cx. pipiens biotype molestus, from left to right: a 100 bp size marker, 1 Cx. pipiens biotype pipiens (control), 11 Cx. pipiens biotype molestus collected in Gothenburg

Thus, environmental characteristics (homodynamic and mammalophilic), as well as molecular identification confirm the first report of presence of Cx. pipiens biotype molestus in Sweden. As of yet, however, no larval habitat has been identified.

This is the first time that a species of Culex has been reported to cause nuisance in Scandinavia. The most common Culex species in Sweden, Cx. torrentium, is often infected with SINV and is also a very efficient enzootic vector of the virus among birds [11, 12]. For transmission to humans to occur, it is also necessary to have a competent bridge vector that feeds opportunistically on both birds and humans. The discovery of Cx. pipiens biotype molestus in a densely populated area Sweden is important, as the presence of a bridge vector may increase the transmission risk of endemic SINV, as well as the risk for introduction and establishment of WNV and USUV. In addition to its vector potential, Cx. pipiens biotype molestus causes severe nuisance to humans, biting usually during night-time.

The origin of the Swedish Cx. pipiens biotype molestus is unknown. Population genetics studies have shown that populations of Cx. pipiens biotype molestus from different European countries are more closely related to each other than to nearby Cx. pipiens biotype pipiens populations [1, 2, 4, 6]. Thus Cx. pipiens biotype molestus is considered by most authors to be introduced into an area, rather than evolving through an adaptation of local Cx. pipiens biotype pipiens populations. The ways of introduction of Cx. pipiens biotype molestus to Sweden, and its distribution, will be further investigated. These are important steps towards a realistic risk assessment for mosquito-borne virus transmission to humans in Scandinavia.

Declarations

Acknowledgements

We are grateful to the members of the affected housing cooperative who help out in collecting household data and mosquito samples.

Funding

Not applicable

Availability of data and materials

Not applicable

Authors’ contributions

JH performed sampling and molecular analysis, and wrote the manuscript, MS and JL initiated the study, and read and commented on the manuscript. All authors read and approved the final manuscript.

Competing interests

The authors declare that they have no competing interests.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Open AccessThis 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.

Authors’ Affiliations

(1)
Department of Medical Biochemistry and Microbiology (IMBIM), Zoonotic Science Center, Uppsala University
(2)
Department of Epidemiology and Population Health, Institute of Infection and Global Health, University of Liverpool
(3)
Swedish Biological Mosquito Control Project, Nedre Dalälvens Utvecklings AB

References

  1. Becker N, Jöst A, Weitzel T. The Culex pipiens complex in Europe. J Am Mosq Control Assoc. 2012;28(4s):53–67.View ArticlePubMedGoogle Scholar
  2. Byrne K, Nichols RA. Culex pipiens in London underground tunnels: differentiation between surface and subterranean populations. Heredity. 1999;82(1):7–15.View ArticlePubMedGoogle Scholar
  3. Gomes B, Sousa CA, Novo MT, Freitas FB, Alves R, Côrte-Real AR, et al. Asymmetric introgression between sympatric molestus and pipiens forms of Culex pipiens (Diptera: Culicidae) in the Comporta region, Portugal. BMC Evol Biol. 2009;9(1):262.View ArticlePubMedPubMed CentralGoogle Scholar
  4. Rudolf M, Czajka C, Börstler J, Melaun C, Jöst H, von Thien H, et al. First nationwide surveillance of Culex pipiens complex and Culex torrentium mosquitoes demonstrated the presence of Culex pipiens biotype pipiens/molestus hybrids in Germany. PLoS One. 2013;8(9):e71832.View ArticlePubMedPubMed CentralGoogle Scholar
  5. Fortuna C, Remoli ME, Di Luca M, Severini F, Toma L, Benedetti E, et al. Experimental studies on comparison of the vector competence of four Italian Culex pipiens populations for West Nile virus. Parasit Vectors. 2015;8:463.View ArticlePubMedPubMed CentralGoogle Scholar
  6. Fonseca DM, Keyghobadi N, Malcolm CA, Mehmet C, Schaffner F, Mogi M, et al. Emerging vectors in the Culex pipiens complex. Science. 2004;303(5663):1535–8.View ArticlePubMedGoogle Scholar
  7. Lundström JO, Schäfer ML, Hesson JC, Blomgren E, Lindström A, Wahlqvist P, et al. The geographic distribution of mosquito species in Sweden. J Eur Mosq Control Assoc. 2013;31:21–35.Google Scholar
  8. Press release Swedish Veterinary Institute. Available from http://www.sva.se/om-sva/pressrum/nyheter-fran-sva/nilfebersmyggan-upptackt-i-skane (In Swedish). Accessed 11 Nov 2016.
  9. Hesson JC, Lundström JO, Halvarsson P, Erixon P, Collado A. A sensitive and reliable restriction enzyme assay to distinguish between the mosquitoes Culex torrentium and Culex pipiens. Med Vet Entomol. 2010;24:142–9.View ArticlePubMedGoogle Scholar
  10. Bahnck CM, Fonseca DM. Rapid assay to identify the two genetic forms of Culex (Culex) pipiens L. (Diptera: Culicidae) and hybrid populations. Am J Trop Med Hyg. 2006;75(2):251–5.PubMedGoogle Scholar
  11. Lundström JO, Niklasson B, Francy DB. Swedish Culex torrentium and Cx. pipiens (Diptera:Culicidae) as experimental vectors of Ockelbo virus. J Med Entomol. 1990;27:561–3.View ArticlePubMedGoogle Scholar
  12. Hesson JC, Verner-Carlsson J, Larsson A, Ahmed R, Lundkvist Å, Lundström JO. Culex torrentium mosquito role as major enzootic vector defined by rate of Sindbis virus infection, Sweden, 2009. Emerg Infect Dis. 2015;21:875–8.View ArticlePubMedPubMed CentralGoogle Scholar

Copyright

© The Author(s). 2016

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Advertisement