Skip to main content
Top
Published in: Malaria Journal 1/2009

Open Access 01-12-2009 | Research

Cultured skin microbiota attracts malaria mosquitoes

Authors: Niels O Verhulst, Hans Beijleveld, Bart GJ Knols, Willem Takken, Gosse Schraa, Harro J Bouwmeester, Renate C Smallegange

Published in: Malaria Journal | Issue 1/2009

Login to get access

Abstract

Background

Host-seeking of the African malaria mosquito, Anopheles gambiae sensu stricto, is guided by human odours. The precise nature of the odours, and the composition of attractive blends of volatiles, remains largely unknown. Skin microbiota plays an important role in the production of human body odours. It is hypothesized that host attractiveness and selection of An. gambiae is affected by the species composition, density, and metabolic activity of the skin microbiota. A study is presented in which the production and constituency of volatile organic compounds (VOCs) by human skin microbiota is examined and the behavioural responses of An. gambiae to VOCs from skin microbiota are investigated.

Methods

Blood agar plates incubated with skin microbiota from human feet or with a reference strain of Staphylococcus epidermidis were tested for their attractiveness to An. gambiae in olfactometer bioassays and indoor trapping experiments. Entrained air collected from blood agar plates incubated with natural skin microbiota or with S. epidermidis were analysed using GC-MS. A synthetic blend of the compounds identified was tested for its attractiveness to An. gambiae. Behavioural data were analysed by a χ2-test and GLM. GC-MS results were analysed by fitting an exponential regression line to test the effect of the concentration of bacteria.

Results

More An. gambiae were caught with blood agar plates incubated with skin bacteria than with sterile blood agar plates, with a significant effect of incubation time and dilution of the skin microbiota. When bacteria from the feet of four other volunteers were tested, similar effects were found. Fourteen putative attractants were found in the headspace of the skin bacteria. A synthetic blend of 10 of these was attractive to An. gambiae.

Conclusions

The discovery that volatiles produced by human skin microorganisms in vitro mediate An. gambiae host-seeking behaviour creates new opportunities for the development of odour-baited trapping systems. Additionally, identification of bacterial volatiles provides a new method to develop synthetic blends, attractive to An. gambiae and possibly other anthropophilic disease vectors.
Appendix
Available only for authorised users
Literature
1.
go back to reference Takken W, Knols BG: Odor-mediated behavior of afrotropical malaria mosquitoes. Annu Rev Entomol. 1999, 44: 131-157. 10.1146/annurev.ento.44.1.131.CrossRefPubMed Takken W, Knols BG: Odor-mediated behavior of afrotropical malaria mosquitoes. Annu Rev Entomol. 1999, 44: 131-157. 10.1146/annurev.ento.44.1.131.CrossRefPubMed
2.
go back to reference Kelly DW: Why are some people bitten more than others?. Trends Parasitol. 2001, 17: 578-581. 10.1016/S1471-4922(01)02116-X.CrossRefPubMed Kelly DW: Why are some people bitten more than others?. Trends Parasitol. 2001, 17: 578-581. 10.1016/S1471-4922(01)02116-X.CrossRefPubMed
3.
go back to reference Qiu YT, Smallegange RC, Van Loon JJA, Ter Braak CJF, Takken W: Interindividual variation in the attractiveness of human odours to the malaria mosquito Anopheles gambiae s. s. Med Vet Entomol. 2006, 20: 280-287. 10.1111/j.1365-2915.2006.00627.x.CrossRefPubMed Qiu YT, Smallegange RC, Van Loon JJA, Ter Braak CJF, Takken W: Interindividual variation in the attractiveness of human odours to the malaria mosquito Anopheles gambiae s. s. Med Vet Entomol. 2006, 20: 280-287. 10.1111/j.1365-2915.2006.00627.x.CrossRefPubMed
4.
go back to reference Logan JG, Birkett MA, Clark SJ, Powers S, Seal NJ, Wadhams LJ, Mordue AJ, Pickett JA: Identification of human-derived volatile chemicals that Interfere with attraction of Aedes aegypti m osquitoes. J Chem Ecol. 2008, 34: 308-322. 10.1007/s10886-008-9436-0.CrossRefPubMed Logan JG, Birkett MA, Clark SJ, Powers S, Seal NJ, Wadhams LJ, Mordue AJ, Pickett JA: Identification of human-derived volatile chemicals that Interfere with attraction of Aedes aegypti m osquitoes. J Chem Ecol. 2008, 34: 308-322. 10.1007/s10886-008-9436-0.CrossRefPubMed
5.
go back to reference Leyden JJ, McGinley KJ, Holzle E, Labows JN, Kligman AM: The microbiology of the human axilla and its relationship to axillary odor. J Investig Dermatol. 1981, 77: 413-416. 10.1111/1523-1747.ep12494624.CrossRefPubMed Leyden JJ, McGinley KJ, Holzle E, Labows JN, Kligman AM: The microbiology of the human axilla and its relationship to axillary odor. J Investig Dermatol. 1981, 77: 413-416. 10.1111/1523-1747.ep12494624.CrossRefPubMed
6.
go back to reference Shelley WWB, Hurley HHJ, Nichols AAC: Axillary odor; experimental study of the role of bacteria, apocrine sweat, and deodorants. AMA Arch Derm Syphilol. 1953, 68: 430-446.CrossRefPubMed Shelley WWB, Hurley HHJ, Nichols AAC: Axillary odor; experimental study of the role of bacteria, apocrine sweat, and deodorants. AMA Arch Derm Syphilol. 1953, 68: 430-446.CrossRefPubMed
7.
go back to reference Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B: Bacterial volatiles and their action potential. Appl Microbiol Biotechnol. 2009, 81: 1001-1012. 10.1007/s00253-008-1760-3.CrossRefPubMed Kai M, Haustein M, Molina F, Petri A, Scholz B, Piechulla B: Bacterial volatiles and their action potential. Appl Microbiol Biotechnol. 2009, 81: 1001-1012. 10.1007/s00253-008-1760-3.CrossRefPubMed
8.
go back to reference Marshall J, Holland KT, Gribbon EM: A comparative-study of the cutaneous microflora of normal feet with low and high-Levels of odor. J Appl Bacteriol. 1988, 65: 61-68.CrossRefPubMed Marshall J, Holland KT, Gribbon EM: A comparative-study of the cutaneous microflora of normal feet with low and high-Levels of odor. J Appl Bacteriol. 1988, 65: 61-68.CrossRefPubMed
9.
go back to reference Xu Y, Dixon S, Brereton R, Soini H, Novotny M, Trebesius K, Bergmaier I, Oberzaucher E, Grammer K, Penn D: Comparison of human axillary odour profiles obtained by gas chromatography/mass spectrometry and skin microbial profiles obtained by denaturing gradient gel electrophoresis using multivariate pattern recognition. Metabolomics. 2007, 3: 427-437. 10.1007/s11306-007-0054-6.CrossRef Xu Y, Dixon S, Brereton R, Soini H, Novotny M, Trebesius K, Bergmaier I, Oberzaucher E, Grammer K, Penn D: Comparison of human axillary odour profiles obtained by gas chromatography/mass spectrometry and skin microbial profiles obtained by denaturing gradient gel electrophoresis using multivariate pattern recognition. Metabolomics. 2007, 3: 427-437. 10.1007/s11306-007-0054-6.CrossRef
10.
go back to reference Smith T, Maire N, Dietz K, Killeen GF, Vounatsou P, Molineaux L, Tanner M: Relationship between the entomological inoculation rate and the force of infection for Plasmodium falciparum malaria. Am J Trop Med Hyg. 2006, 75: 11-18.PubMed Smith T, Maire N, Dietz K, Killeen GF, Vounatsou P, Molineaux L, Tanner M: Relationship between the entomological inoculation rate and the force of infection for Plasmodium falciparum malaria. Am J Trop Med Hyg. 2006, 75: 11-18.PubMed
11.
go back to reference Knols BG, van Loon JJ, Cork A, Robinson RD, Adam W, Meijerink J, de Jong R, Takken W: Behavioural and electrophysiological responses of the female malaria mosquito Anopheles gambiae (Diptera: Culicidae) to Limburger cheese volatiles. Bull Entomol Res. 1997, 87: 151-159. 10.1017/S0007485300027292.CrossRef Knols BG, van Loon JJ, Cork A, Robinson RD, Adam W, Meijerink J, de Jong R, Takken W: Behavioural and electrophysiological responses of the female malaria mosquito Anopheles gambiae (Diptera: Culicidae) to Limburger cheese volatiles. Bull Entomol Res. 1997, 87: 151-159. 10.1017/S0007485300027292.CrossRef
12.
go back to reference Knols BG, De Jong R: Limburger cheese as an attractant for the mosquito Anopheles gambiae s. s. Parasitol Today. 1996, 12: 159-161. 10.1016/0169-4758(96)10002-8.CrossRefPubMed Knols BG, De Jong R: Limburger cheese as an attractant for the mosquito Anopheles gambiae s. s. Parasitol Today. 1996, 12: 159-161. 10.1016/0169-4758(96)10002-8.CrossRefPubMed
13.
go back to reference Knols BG, Meijerink J: Odors influence mosquito behavior. Science and Medicine. 1997, 56-63. Knols BG, Meijerink J: Odors influence mosquito behavior. Science and Medicine. 1997, 56-63.
14.
go back to reference Braks MA, Takken W: Incubated human sweat but not fresh sweat attracts the malaria mosquito Anopheles gambiae sensu stricto. J Chem Ecol. 1999, 25: 663-672. 10.1023/A:1020970307748.CrossRef Braks MA, Takken W: Incubated human sweat but not fresh sweat attracts the malaria mosquito Anopheles gambiae sensu stricto. J Chem Ecol. 1999, 25: 663-672. 10.1023/A:1020970307748.CrossRef
15.
go back to reference Bernier UR, Kline DL, Barnard DR, Schreck CE, Yost RA: Analysis of human skin emanations by gas chromatography/mass spectrometry. 2. Identification of volatile compounds that are candidate attractants for yellow fever mosquito (Aedes aegypti). Anal Chem. 2000, 72: 747-756. 10.1021/ac990963k.CrossRefPubMed Bernier UR, Kline DL, Barnard DR, Schreck CE, Yost RA: Analysis of human skin emanations by gas chromatography/mass spectrometry. 2. Identification of volatile compounds that are candidate attractants for yellow fever mosquito (Aedes aegypti). Anal Chem. 2000, 72: 747-756. 10.1021/ac990963k.CrossRefPubMed
16.
go back to reference Meijerink J, Braks MAH, Brack AA, Adam W, Dekker T, Posthumus MA, Beek TAv, Loon JJAv: Identification of olfactory stimulants for Anopheles gambiae from human sweat samples. J Chem Ecol. 2000, 26: 1367-1382. 10.1023/A:1005475422978.CrossRef Meijerink J, Braks MAH, Brack AA, Adam W, Dekker T, Posthumus MA, Beek TAv, Loon JJAv: Identification of olfactory stimulants for Anopheles gambiae from human sweat samples. J Chem Ecol. 2000, 26: 1367-1382. 10.1023/A:1005475422978.CrossRef
17.
go back to reference Dicke M, Sabelis MW: Infochemical terminology: based on cost-benefit analysis rather than origin of compounds?. Funct Ecol. 1988, 2: 131-139. 10.2307/2389687.CrossRef Dicke M, Sabelis MW: Infochemical terminology: based on cost-benefit analysis rather than origin of compounds?. Funct Ecol. 1988, 2: 131-139. 10.2307/2389687.CrossRef
18.
go back to reference Dethier VG, Browne LB, Smith CN: The designation of chemicals in terms of the responses they elicit from insects. J Econ Entomol. 1960, 53: 134-136.CrossRef Dethier VG, Browne LB, Smith CN: The designation of chemicals in terms of the responses they elicit from insects. J Econ Entomol. 1960, 53: 134-136.CrossRef
19.
go back to reference De Jong R, Knols BGJ: Selection of biting sites on man by two malaria mosquito species. Experientia. 1995, 51: 80-84. 10.1007/BF01964925.CrossRefPubMed De Jong R, Knols BGJ: Selection of biting sites on man by two malaria mosquito species. Experientia. 1995, 51: 80-84. 10.1007/BF01964925.CrossRefPubMed
20.
go back to reference Taylor D, Daulby A, Grimshaw S, James G, Mercer J, Vaziri S: Characterization of the microflora of the human axilla. Int J Cosmet Sci. 2003, 25: 137-145. 10.1046/j.1467-2494.2003.00181.x.CrossRefPubMed Taylor D, Daulby A, Grimshaw S, James G, Mercer J, Vaziri S: Characterization of the microflora of the human axilla. Int J Cosmet Sci. 2003, 25: 137-145. 10.1046/j.1467-2494.2003.00181.x.CrossRefPubMed
21.
go back to reference Knols BGJ, De Jong R, Takken W: Trapping system for testing olfactory responses of the malaria mosquito Anopheles gambiae in a wind-tunnel. Med Vet Entomol. 1994, 8: 386-388. 10.1111/j.1365-2915.1994.tb00104.x.CrossRefPubMed Knols BGJ, De Jong R, Takken W: Trapping system for testing olfactory responses of the malaria mosquito Anopheles gambiae in a wind-tunnel. Med Vet Entomol. 1994, 8: 386-388. 10.1111/j.1365-2915.1994.tb00104.x.CrossRefPubMed
22.
go back to reference Smallegange RC, Qiu YT, van Loon JJ, Takken W: Synergism between ammonia, lactic acid and carboxylic acids as kairomones in the host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto (Diptera: Culicidae). Chem Senses. 2005, 30: 145-152. 10.1093/chemse/bji010.CrossRefPubMed Smallegange RC, Qiu YT, van Loon JJ, Takken W: Synergism between ammonia, lactic acid and carboxylic acids as kairomones in the host-seeking behaviour of the malaria mosquito Anopheles gambiae sensu stricto (Diptera: Culicidae). Chem Senses. 2005, 30: 145-152. 10.1093/chemse/bji010.CrossRefPubMed
23.
go back to reference Maxwell CA, Wakibara J, Tho S, Curtis CF: Malaria-infective biting at different hours of the night. Med Vet Entomol. 1998, 12: 325-327. 10.1046/j.1365-2915.1998.00108.x.CrossRefPubMed Maxwell CA, Wakibara J, Tho S, Curtis CF: Malaria-infective biting at different hours of the night. Med Vet Entomol. 1998, 12: 325-327. 10.1046/j.1365-2915.1998.00108.x.CrossRefPubMed
24.
go back to reference Killeen G, Kihonda J, Lyimo E, Oketch F, Kotas M, Mathenge E, Schellenberg J, Lengeler C, Smith T, Drakeley C: Quantifying behavioural interactions between humans and mosquitoes: Evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006, 6: 161-10.1186/1471-2334-6-161.PubMedCentralCrossRefPubMed Killeen G, Kihonda J, Lyimo E, Oketch F, Kotas M, Mathenge E, Schellenberg J, Lengeler C, Smith T, Drakeley C: Quantifying behavioural interactions between humans and mosquitoes: Evaluating the protective efficacy of insecticidal nets against malaria transmission in rural Tanzania. BMC Infect Dis. 2006, 6: 161-10.1186/1471-2334-6-161.PubMedCentralCrossRefPubMed
25.
go back to reference Healy TP, Copland MJW: Human sweat and 2-oxopentanoic acid elicid a landing response from Anopheles gambiae. Med Vet Entomol. 2000, 14: 195-200. 10.1046/j.1365-2915.2000.00238.x.CrossRefPubMed Healy TP, Copland MJW: Human sweat and 2-oxopentanoic acid elicid a landing response from Anopheles gambiae. Med Vet Entomol. 2000, 14: 195-200. 10.1046/j.1365-2915.2000.00238.x.CrossRefPubMed
26.
go back to reference Noble WC: The skin microflora and microbial skin disease. 2004, Cambridge University Press Noble WC: The skin microflora and microbial skin disease. 2004, Cambridge University Press
27.
go back to reference Kline DL: Comparison of two American mosquito traps: the professional and a new counterflow geometry trap. J Am Mosq Control Assoc. 1999, 15: 276-282.PubMed Kline DL: Comparison of two American mosquito traps: the professional and a new counterflow geometry trap. J Am Mosq Control Assoc. 1999, 15: 276-282.PubMed
28.
go back to reference Torr SJ, Hall DR, Phelps RJ, Vale GA: Methods for dispensing odour attractants for tsetse flies (Diptera: Glossinidae). Bull Entomol Res. 1997, 87: 299-311. 10.1017/S0007485300037251.CrossRef Torr SJ, Hall DR, Phelps RJ, Vale GA: Methods for dispensing odour attractants for tsetse flies (Diptera: Glossinidae). Bull Entomol Res. 1997, 87: 299-311. 10.1017/S0007485300037251.CrossRef
29.
go back to reference Mboera LE, Takken W: Carbon dioxide chemotropism in mosquitoes (Diptera: Culicidae) and its potential in vector surveillance and management programmes. Rev appl entomol, Ser B. 1997, 85: 355-368. Mboera LE, Takken W: Carbon dioxide chemotropism in mosquitoes (Diptera: Culicidae) and its potential in vector surveillance and management programmes. Rev appl entomol, Ser B. 1997, 85: 355-368.
30.
go back to reference Spitzen J, Smallegange RC, Takken W: Effect of human odours and positioning of CO2 release point on trap catches of the malaria mosquito Anopheles gambiae sensu stricto in an olfactometer. Physiol Entomol. 2008, 33: 116-122. 10.1111/j.1365-3032.2008.00612.x.CrossRef Spitzen J, Smallegange RC, Takken W: Effect of human odours and positioning of CO2 release point on trap catches of the malaria mosquito Anopheles gambiae sensu stricto in an olfactometer. Physiol Entomol. 2008, 33: 116-122. 10.1111/j.1365-3032.2008.00612.x.CrossRef
31.
go back to reference Logan JG, Birkett MA: Semiochemicals for biting fly control: Their identification and exploitation. Pest Manag Sci. 2007, 63: 647-657. 10.1002/ps.1408.CrossRefPubMed Logan JG, Birkett MA: Semiochemicals for biting fly control: Their identification and exploitation. Pest Manag Sci. 2007, 63: 647-657. 10.1002/ps.1408.CrossRefPubMed
32.
go back to reference Allan SA, Bernier UR, Kline DL: Attraction of mosquitoes to volatiles associated with blood. J Vector Ecol. 2006, 31 (1): 71-78. 10.3376/1081-1710(2006)31[71:AOMTVA]2.0.CO;2.CrossRefPubMed Allan SA, Bernier UR, Kline DL: Attraction of mosquitoes to volatiles associated with blood. J Vector Ecol. 2006, 31 (1): 71-78. 10.3376/1081-1710(2006)31[71:AOMTVA]2.0.CO;2.CrossRefPubMed
33.
go back to reference Marshall J, Leeming JP, Holland KT: The cutaneous microbiology of normal feet. J Appl Bacteriol. 1987, 62: 139-146.CrossRefPubMed Marshall J, Leeming JP, Holland KT: The cutaneous microbiology of normal feet. J Appl Bacteriol. 1987, 62: 139-146.CrossRefPubMed
34.
go back to reference James AG, Hyliands D, Johnston H: Generation of volatile fatty acids by axillary bacteria. Int J Cosmet Sci. 2004, 26: 149-156. 10.1111/j.1467-2494.2004.00214.x.CrossRefPubMed James AG, Hyliands D, Johnston H: Generation of volatile fatty acids by axillary bacteria. Int J Cosmet Sci. 2004, 26: 149-156. 10.1111/j.1467-2494.2004.00214.x.CrossRefPubMed
35.
go back to reference Ara K, Hama M, Akiba S, Koike K, Okisaka K, Hagura T, Kamiya T, Tomita F: Foot odor due to microbial metabolism and its control. Can J Microbiol. 2006, 52: 357-364. 10.1139/W05-130.CrossRefPubMed Ara K, Hama M, Akiba S, Koike K, Okisaka K, Hagura T, Kamiya T, Tomita F: Foot odor due to microbial metabolism and its control. Can J Microbiol. 2006, 52: 357-364. 10.1139/W05-130.CrossRefPubMed
36.
go back to reference James AG, Casey J, Hyliands D, Mycock G: Fatty acid metabolism by cutaneous bacteria and its role in axillary malodour. World J Microbiol Biotechnol. 2004, 20: 787-10.1007/s11274-004-5843-8.CrossRef James AG, Casey J, Hyliands D, Mycock G: Fatty acid metabolism by cutaneous bacteria and its role in axillary malodour. World J Microbiol Biotechnol. 2004, 20: 787-10.1007/s11274-004-5843-8.CrossRef
37.
go back to reference Gower DB, Holland KT, Mallet AI, Rennie PJ, Watkins WJ: Comparison of 16-Androstene steroid concentrations in sterile Apocrine sweat and Axillary secretions: Interconversions of 16-Androstenes by the Axillary microflora - a mechanism for Axillary odour production in man?. J Steroid Biochem Mol Biol. 1994, 48: 409-418. 10.1016/0960-0760(94)90082-5.CrossRefPubMed Gower DB, Holland KT, Mallet AI, Rennie PJ, Watkins WJ: Comparison of 16-Androstene steroid concentrations in sterile Apocrine sweat and Axillary secretions: Interconversions of 16-Androstenes by the Axillary microflora - a mechanism for Axillary odour production in man?. J Steroid Biochem Mol Biol. 1994, 48: 409-418. 10.1016/0960-0760(94)90082-5.CrossRefPubMed
38.
go back to reference Qiu YT: Sensory and behavioural responses of the malaria mosquito Anopheles gambiae to human odours. 2005, Wageningen University Qiu YT: Sensory and behavioural responses of the malaria mosquito Anopheles gambiae to human odours. 2005, Wageningen University
39.
go back to reference Bernier UR, Booth MM, Yost RA: Analysis of human skin emanations by gas chromatography/mass spectrometry. 1. Thermal desorption of attractants for the yellow fever mosquito (Aedes aegypti) from handled glass beads. Anal Chem. 1999, 71: 1-7. 10.1021/ac980990v.CrossRefPubMed Bernier UR, Booth MM, Yost RA: Analysis of human skin emanations by gas chromatography/mass spectrometry. 1. Thermal desorption of attractants for the yellow fever mosquito (Aedes aegypti) from handled glass beads. Anal Chem. 1999, 71: 1-7. 10.1021/ac980990v.CrossRefPubMed
40.
go back to reference Curran AM, Rabin SI, Prada PA, Furton KG: Comparison of the volatile organic compounds present in human odor using SPME-GC/MS. J Chem Ecol. 2005, 31: 1607-1619. 10.1007/s10886-005-5801-4.CrossRefPubMed Curran AM, Rabin SI, Prada PA, Furton KG: Comparison of the volatile organic compounds present in human odor using SPME-GC/MS. J Chem Ecol. 2005, 31: 1607-1619. 10.1007/s10886-005-5801-4.CrossRefPubMed
41.
go back to reference Gallagher M, Wysocki CJ, Leyden JJ, Spielman AI, Sun X, Preti G: Analyses of volatile organic compounds from human skin. Br J Dermatol. 2008, 159: 780-791. 10.1111/j.1365-2133.2008.08748.x.PubMedCentralCrossRefPubMed Gallagher M, Wysocki CJ, Leyden JJ, Spielman AI, Sun X, Preti G: Analyses of volatile organic compounds from human skin. Br J Dermatol. 2008, 159: 780-791. 10.1111/j.1365-2133.2008.08748.x.PubMedCentralCrossRefPubMed
42.
go back to reference Njiru B, Mukabana W, Takken W, Knols B: Trapping of the malaria vector Anopheles gambiae with odour-baited MM-X traps in semi-field conditions in western Kenya. Malar J. 2006, 5: 39-10.1186/1475-2875-5-39.PubMedCentralCrossRefPubMed Njiru B, Mukabana W, Takken W, Knols B: Trapping of the malaria vector Anopheles gambiae with odour-baited MM-X traps in semi-field conditions in western Kenya. Malar J. 2006, 5: 39-10.1186/1475-2875-5-39.PubMedCentralCrossRefPubMed
43.
go back to reference Qiu YT, Smallegange RC, Ter Braak CJF, Spitzen J, Van Loon JJA, Jawara M, Milligan P, Galimard AM, Van Beek TA, Knols BGJ: Attractiveness of MM-X traps baited with human or synthetic odor to mosquitoes (Diptera: Culicidae) in the Gambia. J Med Entomol. 2007, 44: 970-983. 10.1603/0022-2585(2007)44[970:AOMTBW]2.0.CO;2.PubMedCentralCrossRefPubMed Qiu YT, Smallegange RC, Ter Braak CJF, Spitzen J, Van Loon JJA, Jawara M, Milligan P, Galimard AM, Van Beek TA, Knols BGJ: Attractiveness of MM-X traps baited with human or synthetic odor to mosquitoes (Diptera: Culicidae) in the Gambia. J Med Entomol. 2007, 44: 970-983. 10.1603/0022-2585(2007)44[970:AOMTBW]2.0.CO;2.PubMedCentralCrossRefPubMed
44.
go back to reference Jawara M, Smallegange RC, Jeffries D, Nwakanma DC, Awolola TS, Knols BGJ, Takken W, Conway DJ: Optimising odour baited trap methods for collecting mosquitoes during the malaria season in The Gambia. PLoS ONE. 2009, 12: e8167-10.1371/journal.pone.0008167.CrossRef Jawara M, Smallegange RC, Jeffries D, Nwakanma DC, Awolola TS, Knols BGJ, Takken W, Conway DJ: Optimising odour baited trap methods for collecting mosquitoes during the malaria season in The Gambia. PLoS ONE. 2009, 12: e8167-10.1371/journal.pone.0008167.CrossRef
45.
go back to reference Vale GA, Hall DR: The use of 1-octen-3-ol, acetone and carbon dioxide to improve baits for tsetse flies, Glossina spp. (Diptera: Glossinidae). Bull Entomol Res. 1985, 75: 219-231. 10.1017/S0007485300014309.CrossRef Vale GA, Hall DR: The use of 1-octen-3-ol, acetone and carbon dioxide to improve baits for tsetse flies, Glossina spp. (Diptera: Glossinidae). Bull Entomol Res. 1985, 75: 219-231. 10.1017/S0007485300014309.CrossRef
46.
go back to reference Bosch OJ, Geier M, Boeckh J: Contribution of fatty acids to olfactory host finding of female Aedes aegypti. Chem Senses. 2000, 25: 323-330.CrossRefPubMed Bosch OJ, Geier M, Boeckh J: Contribution of fatty acids to olfactory host finding of female Aedes aegypti. Chem Senses. 2000, 25: 323-330.CrossRefPubMed
47.
go back to reference Smallegange R, Qiu Y, Bukovinszkiné-Kiss G, Van Loon J, Takken W: The effect of aliphatic carboxylic acids on olfaction-based host-seeking of the malaria mosquito Anopheles gambiae sensu stricto. J Chem Ecol. 2009, 35 (8): 933-943. 10.1007/s10886-009-9668-7.PubMedCentralCrossRefPubMed Smallegange R, Qiu Y, Bukovinszkiné-Kiss G, Van Loon J, Takken W: The effect of aliphatic carboxylic acids on olfaction-based host-seeking of the malaria mosquito Anopheles gambiae sensu stricto. J Chem Ecol. 2009, 35 (8): 933-943. 10.1007/s10886-009-9668-7.PubMedCentralCrossRefPubMed
48.
go back to reference Debboun M, Frances SP, Strickman D: Insect Repellents. Principles, Methods, and Uses. 2007, CRC Press Debboun M, Frances SP, Strickman D: Insect Repellents. Principles, Methods, and Uses. 2007, CRC Press
49.
go back to reference Kline DL: Semiochemicals, traps/targets and mass trapping technology for mosquito management. J Am Mosq Control Assoc. 2007, 23: 241-251. 10.2987/8756-971X(2007)23[241:STAMTT]2.0.CO;2.CrossRefPubMed Kline DL: Semiochemicals, traps/targets and mass trapping technology for mosquito management. J Am Mosq Control Assoc. 2007, 23: 241-251. 10.2987/8756-971X(2007)23[241:STAMTT]2.0.CO;2.CrossRefPubMed
Metadata
Title
Cultured skin microbiota attracts malaria mosquitoes
Authors
Niels O Verhulst
Hans Beijleveld
Bart GJ Knols
Willem Takken
Gosse Schraa
Harro J Bouwmeester
Renate C Smallegange
Publication date
01-12-2009
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2009
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-8-302

Other articles of this Issue 1/2009

Malaria Journal 1/2009 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
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 discusses last year's major advances in heart failure and cardiomyopathies.