Skip to main content
Top
Published in: Malaria Journal 1/2012

Open Access 01-12-2012 | Research

Anopheles plumbeus (Diptera: Culicidae) in Europe: a mere nuisance mosquito or potential malaria vector?

Authors: Francis Schaffner, Isabelle Thiéry, Christian Kaufmann, Agnès Zettor, Christian Lengeler, Alexander Mathis, Catherine Bourgouin

Published in: Malaria Journal | Issue 1/2012

Login to get access

Abstract

Background

Anopheles plumbeus has been recognized as a minor vector for human malaria in Europe since the beginning of the 20th century. In recent years this tree hole breeding mosquito species appears to have exploited novel breeding sites, including large and organically rich man-made containers, with consequently larger mosquito populations in close vicinity to humans. This lead to investigate whether current populations of An. plumbeus would be able to efficiently transmit Plasmodium falciparum, the parasite responsible for the most deadly form of malaria.

Methods

Anopheles plumbeus immatures were collected from a liquid manure pit in Switzerland and transferred as adults to the CEPIA (Institut Pasteur, France) where they were fed on P. falciparum gametocytes produced in vitro. Anopheles gambiae mosquitoes served as controls. Development of P. falciparum in both mosquito species was followed by microscopical detection of oocysts on mosquito midguts and by sporozoite detection in the head/thorax by PCR and microscopy.

Results

A total of 293 wild An. plumbeus females from four independent collections successfully fed through a membrane on blood containing P. falciparum gametocytes. Oocysts were observed in mosquito midguts and P. falciparum DNA was detected in head-thorax samples in all four experiments, demonstrating, on a large mosquito sample, that An. plumbeus is indeed receptive to P. falciparum NF54 and able to produce sporozoites. Importantly, the proportion of sporozoites-infected An. plumbeus was almost similar to that of An. gambiae (31 to 88% An. plumbeus versus 67 to 97% An. gambiae). However, the number of sporozoites produced was significantly lower in infected An. plumbeus.

Conclusion

The results show that a sample of field-caught An. plumbeus has a moderate to high receptivity towards P. falciparum. Considering the increased mobility of humans between Europe and malaria endemic countries and changes in environment and climate, these data strongly suggest that An. plumbeus could act as a vector for malaria and thus significantly contribute to increasing the malaria transmission risk in Central-Western Europe. In locations showing high vulnerability to the presence of gametocyte carriers, the risk of transmission of malaria by An. plumbeus should be considered.
Appendix
Available only for authorised users
Literature
2.
go back to reference 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, for the CHIKV study group: Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet. 2007, 370: 1840-1846. 10.1016/S0140-6736(07)61779-6.CrossRefPubMed 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, for the CHIKV study group: Infection with chikungunya virus in Italy: an outbreak in a temperate region. Lancet. 2007, 370: 1840-1846. 10.1016/S0140-6736(07)61779-6.CrossRefPubMed
3.
go back to reference Gould EA, Gallian P, De Lamballerie X, Charrel RN: First cases of autochthonous dengue fever and chikungunya fever in France: from bad dream to reality!. Clin Microbiol Infect. 2010, 16: 1702-1704. 10.1111/j.1469-0691.2010.03386.x.CrossRefPubMed Gould EA, Gallian P, De Lamballerie X, Charrel RN: First cases of autochthonous dengue fever and chikungunya fever in France: from bad dream to reality!. Clin Microbiol Infect. 2010, 16: 1702-1704. 10.1111/j.1469-0691.2010.03386.x.CrossRefPubMed
4.
go back to reference Gjenero-Margan I, Aleraj B, Krajcar D, Lesnikar V, Klobučar A, Pem-Novosel I, Kurečić-Filipović S, Komparak S, Martić R, Đuričić S, Betica-Radić L, Okmadžić J, Vilibić-Čavlek T, Babić-Erceg A, Turković B, Avšić-Županc T, Radić I, Ljubić M, Šarac K, Benić N, Mlinarić-Galinović G: Autochthonous dengue fever in Croatia, August–September. Euro Surveill. 2011, 16: pii=19805- Gjenero-Margan I, Aleraj B, Krajcar D, Lesnikar V, Klobučar A, Pem-Novosel I, Kurečić-Filipović S, Komparak S, Martić R, Đuričić S, Betica-Radić L, Okmadžić J, Vilibić-Čavlek T, Babić-Erceg A, Turković B, Avšić-Županc T, Radić I, Ljubić M, Šarac K, Benić N, Mlinarić-Galinović G: Autochthonous dengue fever in Croatia, August–September. Euro Surveill. 2011, 16: pii=19805-
5.
go back to reference Rasmussen LD, Kristensen B, Kirkeby C, Rasmussen TB, Belsham GJ, Bødker R, Bøtner A: Culicoids as vectors of Schmallenberg virus. Emerg Infect Dis. 2012, 18: 1204-1206.PubMedCentralCrossRefPubMed Rasmussen LD, Kristensen B, Kirkeby C, Rasmussen TB, Belsham GJ, Bødker R, Bøtner A: Culicoids as vectors of Schmallenberg virus. Emerg Infect Dis. 2012, 18: 1204-1206.PubMedCentralCrossRefPubMed
6.
go back to reference Steinmetz HW, Bakonyi T, Weissenbock H, Hatt JM, Eulenberger U, Robert N, Hoop R, Nowotny N: Emergence and establishment of Usutu virus infection in wild and captive avian species in and around Zurich, Switzerland - Genomic and pathologic comparison to other central European outbreaks. Vet Microbiol. 2011, 148: 207-212. 10.1016/j.vetmic.2010.09.018.CrossRefPubMed Steinmetz HW, Bakonyi T, Weissenbock H, Hatt JM, Eulenberger U, Robert N, Hoop R, Nowotny N: Emergence and establishment of Usutu virus infection in wild and captive avian species in and around Zurich, Switzerland - Genomic and pathologic comparison to other central European outbreaks. Vet Microbiol. 2011, 148: 207-212. 10.1016/j.vetmic.2010.09.018.CrossRefPubMed
7.
go back to reference Krüger A, Rech A, Su XZ, Tannich E: Two cases of autochthonous Plasmodium falciparum malaria in Germany with evidence for local transmission by indigenous Anopheles plumbeus. Trop Med Int Health. 2001, 6: 983-985. 10.1046/j.1365-3156.2001.00816.x.CrossRefPubMed Krüger A, Rech A, Su XZ, Tannich E: Two cases of autochthonous Plasmodium falciparum malaria in Germany with evidence for local transmission by indigenous Anopheles plumbeus. Trop Med Int Health. 2001, 6: 983-985. 10.1046/j.1365-3156.2001.00816.x.CrossRefPubMed
8.
go back to reference Alten B, Kampen H, Fontenille D: Malaria in Southern Europe: resurgence from the past?. Emerging pests and vector-borne diseases in Europe. Edited by: Takken W, Knols BG. 2007, Wageningen: Wageningen Academic Publishers, 35-57. Alten B, Kampen H, Fontenille D: Malaria in Southern Europe: resurgence from the past?. Emerging pests and vector-borne diseases in Europe. Edited by: Takken W, Knols BG. 2007, Wageningen: Wageningen Academic Publishers, 35-57.
9.
go back to reference Zoller T, Naucke TJ, May J, Hoffmeister B, Flick H, Williams CJ, Frank C, Bergmann F, Suttorp N, Mockenhaupt FP: Malaria transmission in non-endemic areas: case report, review of the literature and implications for public health management. Malar J. 2009, 8: 71-10.1186/1475-2875-8-71.PubMedCentralCrossRefPubMed Zoller T, Naucke TJ, May J, Hoffmeister B, Flick H, Williams CJ, Frank C, Bergmann F, Suttorp N, Mockenhaupt FP: Malaria transmission in non-endemic areas: case report, review of the literature and implications for public health management. Malar J. 2009, 8: 71-10.1186/1475-2875-8-71.PubMedCentralCrossRefPubMed
10.
go back to reference Santa-Olalla Peralta P, Vazquez-Torres MC, Latorre-Fandos E, Mairal-Claver P, Cortina-Solano P, Puy-Azón A, Adiego Sancho B, Leitmeyer K, Lucientes-Curdi J, Sierra-Moros MJ: First autochthonous malaria case due to Plasmodium vivax since eradication, Spain, October 2010. Euro Surveill. 2010, 15: pii=19684- Santa-Olalla Peralta P, Vazquez-Torres MC, Latorre-Fandos E, Mairal-Claver P, Cortina-Solano P, Puy-Azón A, Adiego Sancho B, Leitmeyer K, Lucientes-Curdi J, Sierra-Moros MJ: First autochthonous malaria case due to Plasmodium vivax since eradication, Spain, October 2010. Euro Surveill. 2010, 15: pii=19684-
11.
go back to reference Danis K, Baka A, Lenglet A, Van Bortel W, Terzaki I, Tseroni M, Detsis M, Papanikolaou E, Balaska A, Gewehr S, Dougas G, Sideroglou T, Economopoulou A, Vakalis N, Tsiodras S, Bonovas S, Kremastinou J: Autochthonous Plasmodium vivax malaria in Greece, 2011. Euro Surveill. 2011, 16: pii=19993- Danis K, Baka A, Lenglet A, Van Bortel W, Terzaki I, Tseroni M, Detsis M, Papanikolaou E, Balaska A, Gewehr S, Dougas G, Sideroglou T, Economopoulou A, Vakalis N, Tsiodras S, Bonovas S, Kremastinou J: Autochthonous Plasmodium vivax malaria in Greece, 2011. Euro Surveill. 2011, 16: pii=19993-
12.
go back to reference Randolph SE, Rogers DJ: The arrival, establishment and spread of exotic diseases: patterns and predictions. Nat Rev Microbiol. 2010, 8: 361-371. 10.1038/nrmicro2336.CrossRefPubMed Randolph SE, Rogers DJ: The arrival, establishment and spread of exotic diseases: patterns and predictions. Nat Rev Microbiol. 2010, 8: 361-371. 10.1038/nrmicro2336.CrossRefPubMed
13.
go back to reference Bruce-Chwatt LJ, De Zulueta J: The rise and fall of malaria in Europe: A historico-epidemiological study. 1980, Oxford: Oxford University Press Bruce-Chwatt LJ, De Zulueta J: The rise and fall of malaria in Europe: A historico-epidemiological study. 1980, Oxford: Oxford University Press
14.
go back to reference Hackett LW: Malaria in Europe. An ecological study. 1937, London: Oxford University Press Hackett LW: Malaria in Europe. An ecological study. 1937, London: Oxford University Press
15.
go back to reference Zahar AR: Vector bionomics in the epidemiology and control of malaria. Part II. The WHO European Region & the WHO Eastern Mediterranean Region. Vol II: Applied field studies. 1990, Geneva: World Health Organisation Zahar AR: Vector bionomics in the epidemiology and control of malaria. Part II. The WHO European Region & the WHO Eastern Mediterranean Region. Vol II: Applied field studies. 1990, Geneva: World Health Organisation
16.
go back to reference Schaffner F, Angel G, Geoffroy B, Hervy J-P, Rhaiem A, Brunhes J: The Mosquitoes of Europe. An identification and training programme. 2001, Montpellier: IRD Editions & EID Méditerranée, CD-Rom Schaffner F, Angel G, Geoffroy B, Hervy J-P, Rhaiem A, Brunhes J: The Mosquitoes of Europe. An identification and training programme. 2001, Montpellier: IRD Editions & EID Méditerranée, CD-Rom
17.
go back to reference Becker N, Petrić D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A: Mosquitoes and their control. 2010, Heidelberg: Springer-Verlag, 2CrossRef Becker N, Petrić D, Zgomba M, Boase C, Madon M, Dahl C, Kaiser A: Mosquitoes and their control. 2010, Heidelberg: Springer-Verlag, 2CrossRef
18.
go back to reference Blazquez J, De Zulueta J: The disappearance of Anopheles labranchiae from Spain. Parassitologia. 1980, 22: 161-163.PubMed Blazquez J, De Zulueta J: The disappearance of Anopheles labranchiae from Spain. Parassitologia. 1980, 22: 161-163.PubMed
19.
go back to reference Romi R, Pierdominici G, Severini C, Tamburro A, Cocchi M, Menichetti D, Pili E, Marchi A: Status of malaria vectors in Italy. J Med Entomol. 1997, 34: 263-271.CrossRefPubMed Romi R, Pierdominici G, Severini C, Tamburro A, Cocchi M, Menichetti D, Pili E, Marchi A: Status of malaria vectors in Italy. J Med Entomol. 1997, 34: 263-271.CrossRefPubMed
20.
go back to reference Daškova NG, Rasnicyn SP: Review of data on susceptibility of mosquitoes in the USSR to imported strains of malaria parasites. Bull World Health Organ. 1982, 60: 893-897.PubMedCentralPubMed Daškova NG, Rasnicyn SP: Review of data on susceptibility of mosquitoes in the USSR to imported strains of malaria parasites. Bull World Health Organ. 1982, 60: 893-897.PubMedCentralPubMed
21.
go back to reference Marchant P, Eling W, van Gemert GJ, Leake CJ, Curtis CF: Could British mosquitoes transmit Falciparum malaria?. Parasitol Today. 1998, 14: 344-345. 10.1016/S0169-4758(98)01274-5.CrossRefPubMed Marchant P, Eling W, van Gemert GJ, Leake CJ, Curtis CF: Could British mosquitoes transmit Falciparum malaria?. Parasitol Today. 1998, 14: 344-345. 10.1016/S0169-4758(98)01274-5.CrossRefPubMed
22.
go back to reference Sousa C: PhD thesis. Malaria vectorial capacity and competence of Anopheles atroparvus Van Thiel, 1927 (Diptera, Culicidae): Implications for the potential re-emergence of malaria in Portugal. 2008, Lisbon: Universidade Nova de Lisboa Sousa C: PhD thesis. Malaria vectorial capacity and competence of Anopheles atroparvus Van Thiel, 1927 (Diptera, Culicidae): Implications for the potential re-emergence of malaria in Portugal. 2008, Lisbon: Universidade Nova de Lisboa
23.
go back to reference Toty C, Barré H, Le Goff G, Larget-Thiéry I, Rahola N, Couret D, Fontenille D: Malaria risk in Corsica, former hot spot of malaria in France. Malar J. 2010, 9: 231-10.1186/1475-2875-9-231.PubMedCentralCrossRefPubMed Toty C, Barré H, Le Goff G, Larget-Thiéry I, Rahola N, Couret D, Fontenille D: Malaria risk in Corsica, former hot spot of malaria in France. Malar J. 2010, 9: 231-10.1186/1475-2875-9-231.PubMedCentralCrossRefPubMed
24.
go back to reference Romi R, Boccolini D, Vallorani R, Severini F, Toma L, Cocchi M, Tamburro A, Messeri G, Crisci A, Angeli L, Costantini R, Raffaelli I, Pontuale G, Thiéry I, Landier A, Le Goff G, Fausto AM, Di Luca M: Assessment of the risk of malaria re-introduction in the Maremma plain (Central Italy) using a multi-factorial approach. Malar J. 2012, 11: 98-10.1186/1475-2875-11-98.PubMedCentralCrossRefPubMed Romi R, Boccolini D, Vallorani R, Severini F, Toma L, Cocchi M, Tamburro A, Messeri G, Crisci A, Angeli L, Costantini R, Raffaelli I, Pontuale G, Thiéry I, Landier A, Le Goff G, Fausto AM, Di Luca M: Assessment of the risk of malaria re-introduction in the Maremma plain (Central Italy) using a multi-factorial approach. Malar J. 2012, 11: 98-10.1186/1475-2875-11-98.PubMedCentralCrossRefPubMed
25.
go back to reference Dekoninck W, Hendrickx F, Van Bortel W, Versteirt V, Coosemans M, Damien D, Hance T, De Clercq EM, Hendrickx G, Schaffner F, Grootaert P: Human induced expanded distribution of Anopheles plumbeus, experimental vector of West Nile virus and a potential vector of human malaria in Belgium. J Med Entomol. 2011, 48: 924-928. 10.1603/ME10235.CrossRefPubMed Dekoninck W, Hendrickx F, Van Bortel W, Versteirt V, Coosemans M, Damien D, Hance T, De Clercq EM, Hendrickx G, Schaffner F, Grootaert P: Human induced expanded distribution of Anopheles plumbeus, experimental vector of West Nile virus and a potential vector of human malaria in Belgium. J Med Entomol. 2011, 48: 924-928. 10.1603/ME10235.CrossRefPubMed
26.
go back to reference Schaffner F: Mosquitoes in used tyres in Europe: species list and larval key. Eur Mosq Bull. 2003, 16: 7-12. Schaffner F: Mosquitoes in used tyres in Europe: species list and larval key. Eur Mosq Bull. 2003, 16: 7-12.
27.
go back to reference Schaffner F, Kaufmann C, Hegglin D, Mathis A: The invasive mosquito Aedes japonicus in Central Europe. Med Vet Entomol. 2009, 23: 448-451. 10.1111/j.1365-2915.2009.00825.x.CrossRefPubMed Schaffner F, Kaufmann C, Hegglin D, Mathis A: The invasive mosquito Aedes japonicus in Central Europe. Med Vet Entomol. 2009, 23: 448-451. 10.1111/j.1365-2915.2009.00825.x.CrossRefPubMed
28.
go back to reference Bueno-Marí R, Jiménez-Peydró R: Anopheles plumbeus Stephens, 1828: a neglected malaria vector in Europe. Malaria Reports. 2011, 1: e2-CrossRef Bueno-Marí R, Jiménez-Peydró R: Anopheles plumbeus Stephens, 1828: a neglected malaria vector in Europe. Malaria Reports. 2011, 1: e2-CrossRef
29.
go back to reference Shute PG, Maryon M: Malaria in England past, present and future. Roy Soc Health J. 1974, 94: 23-29. 10.1177/146642407409400111.CrossRef Shute PG, Maryon M: Malaria in England past, present and future. Roy Soc Health J. 1974, 94: 23-29. 10.1177/146642407409400111.CrossRef
30.
go back to reference Sokolova MI, Snow KR: Malaria vectors in European Russia. Eur Mosq Bull. 2002, 12: 1-6. Sokolova MI, Snow KR: Malaria vectors in European Russia. Eur Mosq Bull. 2002, 12: 1-6.
31.
go back to reference Blacklock B, Carter HF: Further experiments with Anopheles plumbeus Stephens, its infection with P. falciparum in England; Also notes on the apparatus and technique employed. Ann Trop Med Par. 1920, 13: 275-283. Blacklock B, Carter HF: Further experiments with Anopheles plumbeus Stephens, its infection with P. falciparum in England; Also notes on the apparatus and technique employed. Ann Trop Med Par. 1920, 13: 275-283.
32.
go back to reference Eling W, van Gemert G-J, Akinpelu O, Curtis J, Curtis CF: Production of Plasmodium falciparum sporozoites by Anopheles plumbeus. Eur Mosq Bull. 2003, 15: 12-13. Eling W, van Gemert G-J, Akinpelu O, Curtis J, Curtis CF: Production of Plasmodium falciparum sporozoites by Anopheles plumbeus. Eur Mosq Bull. 2003, 15: 12-13.
33.
go back to reference World Health Organization: From malaria control to elimination in the WHO European Region 2006–2015. Regional Strategy. 2006, Copenhagen: World Health Organization, Regional Office for Europe World Health Organization: From malaria control to elimination in the WHO European Region 2006–2015. Regional Strategy. 2006, Copenhagen: World Health Organization, Regional Office for Europe
34.
go back to reference Luterbacher J, Dietrich D, Xoplaki E, Grosjean M, Wanner H: European seasonal and annual temperature variability, trends, and extremes since 1500. Science. 2004, 303: 1499-1503. 10.1126/science.1093877.CrossRefPubMed Luterbacher J, Dietrich D, Xoplaki E, Grosjean M, Wanner H: European seasonal and annual temperature variability, trends, and extremes since 1500. Science. 2004, 303: 1499-1503. 10.1126/science.1093877.CrossRefPubMed
35.
go back to reference Xoplaki E, Luterbacher J, Paeth H, Dietrich D, Steiner N, Grosjean MHW: European spring and autumn temperature variability and change of extremes over the last half millennium. Geophys Res Lett. 2005, 32: L15713-CrossRef Xoplaki E, Luterbacher J, Paeth H, Dietrich D, Steiner N, Grosjean MHW: European spring and autumn temperature variability and change of extremes over the last half millennium. Geophys Res Lett. 2005, 32: L15713-CrossRef
36.
go back to reference Mitri C, Jacques J-C, Thiéry I, Riehle MM, Xu J, Bischoff E, Morlais I, Nsango SE, Vernick KD, Bourgouin C: Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS Pathog. 2009, 5: e1000576-10.1371/journal.ppat.1000576.PubMedCentralCrossRefPubMed Mitri C, Jacques J-C, Thiéry I, Riehle MM, Xu J, Bischoff E, Morlais I, Nsango SE, Vernick KD, Bourgouin C: Fine pathogen discrimination within the APL1 gene family protects Anopheles gambiae against human and rodent malaria species. PLoS Pathog. 2009, 5: e1000576-10.1371/journal.ppat.1000576.PubMedCentralCrossRefPubMed
37.
go back to reference Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C: Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science. 2010, 239: 1353-1355.CrossRef Rodrigues J, Brayner FA, Alves LC, Dixit R, Barillas-Mury C: Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science. 2010, 239: 1353-1355.CrossRef
38.
go back to reference Ponnudurai T, Meuwissen JHET, Leeuwenberg ADEM, Verhave JP, Lensen AHW: The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Trans R Soc Trop Med Hyg. 1982, 76: 242-250. 10.1016/0035-9203(82)90289-9.CrossRefPubMed Ponnudurai T, Meuwissen JHET, Leeuwenberg ADEM, Verhave JP, Lensen AHW: The production of mature gametocytes of Plasmodium falciparum in continuous cultures of different isolates infective to mosquitoes. Trans R Soc Trop Med Hyg. 1982, 76: 242-250. 10.1016/0035-9203(82)90289-9.CrossRefPubMed
39.
go back to reference Mitri C, Thiéry I, Bourgouin C, Paul REL: Density-dependent impact of the human malaria parasite Plasmodium falciparum gametocyte sex ratio on mosquito infection rates. Proc R Soc Biol Sci B. 2009, 276: 3721-3726. 10.1098/rspb.2009.0962.CrossRef Mitri C, Thiéry I, Bourgouin C, Paul REL: Density-dependent impact of the human malaria parasite Plasmodium falciparum gametocyte sex ratio on mosquito infection rates. Proc R Soc Biol Sci B. 2009, 276: 3721-3726. 10.1098/rspb.2009.0962.CrossRef
40.
go back to reference Padley D, Moody AH, Chiodini PL, Saldanha J: Use of a rapid, single-round, multiplex PCR to detect malarial parasites and identify the species present. Ann Trop Med Parasitol. 2003, 97: 131-137. 10.1179/000349803125002977.CrossRefPubMed Padley D, Moody AH, Chiodini PL, Saldanha J: Use of a rapid, single-round, multiplex PCR to detect malarial parasites and identify the species present. Ann Trop Med Parasitol. 2003, 97: 131-137. 10.1179/000349803125002977.CrossRefPubMed
41.
go back to reference Ozaki LS, Gwadz RW, Godson GN: Simple centrifugation method for rapid separation of sporozoites from mosquitoes. J Parasitol. 1984, 70: 831-833. 10.2307/3281779.CrossRefPubMed Ozaki LS, Gwadz RW, Godson GN: Simple centrifugation method for rapid separation of sporozoites from mosquitoes. J Parasitol. 1984, 70: 831-833. 10.2307/3281779.CrossRefPubMed
42.
go back to reference Shute PG: Indigenous P. vivax malaria in London believed to have been transmitted by Anopheles plumbeus. Mon Bull Minist Health Publ Health Lab Serv. 1954, 13: 48-51. Shute PG: Indigenous P. vivax malaria in London believed to have been transmitted by Anopheles plumbeus. Mon Bull Minist Health Publ Health Lab Serv. 1954, 13: 48-51.
43.
go back to reference James SP: The disappearance of malaria from England. Proc R Soc Med. 1929, 23: 1-15. James SP: The disappearance of malaria from England. Proc R Soc Med. 1929, 23: 1-15.
44.
go back to reference Blacklock B, Carter HF: The experimental infection, in England, of Anopheles plumbeus with Plasmodium vivax (sporozoites in salivary glands). Preliminary note. Ann Trop Med Parasitol. 1919, 13: 187-188. Blacklock B, Carter HF: The experimental infection, in England, of Anopheles plumbeus with Plasmodium vivax (sporozoites in salivary glands). Preliminary note. Ann Trop Med Parasitol. 1919, 13: 187-188.
45.
go back to reference Blacklock B, Carter HF: The experimental infection in England, of Anopheles plumbeus Stephens and Anopheles bifurcatus with Plasmodium vivax. Ann Trop Med Parasitol. 1920, 13: 413-420. Blacklock B, Carter HF: The experimental infection in England, of Anopheles plumbeus Stephens and Anopheles bifurcatus with Plasmodium vivax. Ann Trop Med Parasitol. 1920, 13: 413-420.
46.
go back to reference Scott TW, Takken W: Feeding strategies of anthropophilic mosquitoes result in increased risk of pathogen transmission. Trends Parasitol. 2012, 28: 114-121. 10.1016/j.pt.2012.01.001.CrossRefPubMed Scott TW, Takken W: Feeding strategies of anthropophilic mosquitoes result in increased risk of pathogen transmission. Trends Parasitol. 2012, 28: 114-121. 10.1016/j.pt.2012.01.001.CrossRefPubMed
47.
go back to reference Anonymous: Manual on practical entomology in malaria. Part II: Methods and Techniques. 1975, Geneva: World Health Organization Anonymous: Manual on practical entomology in malaria. Part II: Methods and Techniques. 1975, Geneva: World Health Organization
48.
go back to reference Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB: Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA. 2010, 107: 15135-15139. 10.1073/pnas.1006422107.PubMedCentralCrossRefPubMed Paaijmans KP, Blanford S, Bell AS, Blanford JI, Read AF, Thomas MB: Influence of climate on malaria transmission depends on daily temperature variation. Proc Natl Acad Sci USA. 2010, 107: 15135-15139. 10.1073/pnas.1006422107.PubMedCentralCrossRefPubMed
Metadata
Title
Anopheles plumbeus (Diptera: Culicidae) in Europe: a mere nuisance mosquito or potential malaria vector?
Authors
Francis Schaffner
Isabelle Thiéry
Christian Kaufmann
Agnès Zettor
Christian Lengeler
Alexander Mathis
Catherine Bourgouin
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2012
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-11-393

Other articles of this Issue 1/2012

Malaria Journal 1/2012 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.