Advertisement

Analytical and Bioanalytical Chemistry

, Volume 405, Issue 24, pp 7885–7895 | Cite as

A portable electrochemical magnetoimmunosensor for detection of sulfonamide antimicrobials in honey

  • A. Muriano
  • D.-G. Pinacho
  • V. Chabottaux
  • J.-M. Diserens
  • B. Granier
  • S. Stead
  • F. Sanchez Baeza
  • M. I. Pividori
  • M.-P. Marco
Research Paper
Part of the following topical collections:
  1. Rapid Detection in Food and Feed

Abstract

A new electrochemical magnetoimmunosensor (EMIS) has been developed for the screening of residues of sulfonamide antimicrobials in honey samples. The immunosensor is able to detect up to ten different sulfonamide congeners at levels below the action points established in some European countries (25 μg kg−1) after a hydrolysis step in which the sulfonamides are released from the corresponding conjugates formed in samples of this type. In spite of the complexity of the sample after the hydrolysis procedure, the EMIS could perform quantitative measurements, directly in these samples, without any additional sample cleanup or extraction step. For example, sulfapyridine, used as a reference, can be detected in hydrolyzed honey with a limit of detection (IC90) of 0.1 ± 0.03 μg kg−1. Considering that the use of antibiotics for bee treatment is prohibited in the European Union, the immunosensor presented here could be an excellent screening tool. Moreover, several samples can be processed in parallel, which facilitates the analysis, reducing the necessity to use more costly confirmatory methods for just screening. As a proof of concept, a set of blind honey samples (spiked and incurred) were analyzed and the results were compared with those obtained by high-performance liquid chromatography–tandem mass spectrometry, demonstrating the potential of the EMIS as a screening tool.

Keywords

Electrochemical immunosensor Portable biosensor Antimicrobial residues Magnetic beads Honey Sugar hydrolysis 

Notes

Acknowledgments

This work was performed in the frame of European project Conffidence (KBBE-211326). The AMR group (nowadays the Nb4D group) is a consolidated research group (Grup de Recerca) of the Generalitat de Catalunya and has support from the Departament d’Universitats, Recerca I Societat de la informació la Generalitat de Catalunya (expedient 2009 SGR 13432). CIBER-BBN is an initiative funded by the VI National R&D&I Plan 2008–2011, IniciativaIngenio 2010, Consolider Program, CIBER Actions and is financed by the Instituto de Salud Carlos III with assistance from the European Regional Development Foundation.

References

  1. 1.
    Wegener HC (2003) Antibiotics in animal feed and their role in resistance development. Curr Opin Microbiol 6(5):439–445CrossRefGoogle Scholar
  2. 2.
    Hiramatsu K, Cui L, Kuroda M, Ito T (2001) The emergence and evolution of methicillin-resistant Staphylococcus aureus. Trends Microbiol 9(10):486–493CrossRefGoogle Scholar
  3. 3.
    Wang S, Hy Z, Wang L, Duan ZJ, Kennedy I (2006) Analysis of sulphonamide residues in edible animal products: a review. Food Addit Contam 23(4):362–384CrossRefGoogle Scholar
  4. 4.
    Zotou A, Vasiliadou C (2006) Selective determination of sulfonamide residues in honey by SPE-RP-LC with UV detection. Chromatographia 64(5):307–311CrossRefGoogle Scholar
  5. 5.
    Bogdanov S (2005) Contaminants of bee products. Apidologie 37:1–18CrossRefGoogle Scholar
  6. 6.
    Sensderson JP, Naisbitt DJ, Park BK (2006) Role of bioacitvation in drug-induced hypersensitivity reactions. J AAPS 8:E55–E64CrossRefGoogle Scholar
  7. 7.
    Heath JE, Littlefield NA (1984) Morphological effects of subchronic oral sulfamethazine administration on Fischer 344 rats and B6C3F1 mice. Toxicol Pathol 12(1):3–9CrossRefGoogle Scholar
  8. 8.
    Food and Drug Regulations (1991)Table III, Division 15, Part B., Canada Gazette Part II, 125, 1478–1480Google Scholar
  9. 9.
    European Council (1990) Council Regulation (ECC) No 2377/99 of 26 June 1990 laying down a community procedure for the establishment of maximum residue limits of veterinary medicinal products in foodstuffs of animal origin. Off J Eur Communities L224:1Google Scholar
  10. 10.
    Reybroeck W, Daeseleire E, De Brabander HF, Herman L (2012) Antimicrobials in beekeeping. Vet Microbiol 158(1–2):1–11. doi: 10.1016/j.vetmic.2012.01.012 CrossRefGoogle Scholar
  11. 11.
    Bernal J, Nozal MJ, Jiménez JJ, Martín MT, Sanz E (2009) A new and simple method to determine trace levels of sulfonamides in honey by high performance liquid chromatography with fluorescence detection. J Chromatogr A 1216(43):7275–7280. doi: 10.1016/j.chroma.2009.05.046 CrossRefGoogle Scholar
  12. 12.
    Sheridan R, Policastro B, Thomas S, Rice D (2008) Analysis and occurrence of 14 sulfonamide antibacterials and chloramphenicol in honey by solid-phase extraction followed by LC/MS/MS analysis. J Agric Food Chem 56(10):3509–3516CrossRefGoogle Scholar
  13. 13.
    Maudens KE, Zhang G-F, Lambert WE (2004) Quantitative analysis of twelve sulfonamides in honey after acidic hydrolysis by high-performance liquid chromatography with post-column derivatization and fluorescence detection. J Chromatogr A 1047(1):85–92CrossRefGoogle Scholar
  14. 14.
    Pang G-F, Cao Y-Z, Fan C-L, Zhang J-J, Li X-M, Li Z-Y, Jia G-Q (2003) Liquid chromatography–fluorescence detection for simultaneous analysis of sulfonamide residues in honey. Anal Bioanal Chem 376(4):534–54115CrossRefGoogle Scholar
  15. 15.
    Sheth HB, Yaylayan VA, Low NH, Stiles ME, Sporns P (1990) Reaction of reducing sugars with sulfathiazole and importance of this reaction to sulfonamide residue analysis using chromatographic, colorimetric, microbiological, or ELISA methods. J Agric Food Chem 38(4):1125–1130CrossRefGoogle Scholar
  16. 16.
    Heering W, Usleber E, Dietrich D, Märtlbauer E (1998) Immunochemical screening for antimicrobial drug residues in commercial honey. Analyst 123:2759–2762CrossRefGoogle Scholar
  17. 17.
    Schawaiger I, Schuch R (2000) Bound sulfathiazole residues in honey—need of a hydrolysis step for the analytical determination of total sulfathiazole content in honey. Dtsch Lebensmitt Rundsch 96(3):93–98Google Scholar
  18. 18.
    Wang YH, Li L, Chen CH, Cheng SR, Lee MS, Yu PP, Chang-Chien GP (2012) Investigation of breaking efficiency of N-glycosidic bond between sulfonamide and honey. Chem Res Chin Univ 28(2):195–199Google Scholar
  19. 19.
    Adrian J, Fernández F, Muriano A, Obregón R, Ramón J, Tort N, Marco M-P (2010) Immunochemical analytical methods for monitoring the aquatic environments. In: Namiesni J, Szefer P (eds) Analytical methods in aquatic environments. IWA Publishing, LondonGoogle Scholar
  20. 20.
    Nesterenko I, Nokel M, Eremin S (2009) Immunochemical methods for the detection of sulfanylamide drugs. J Anal Chem 64(5):435–444CrossRefGoogle Scholar
  21. 21.
    Fernández F, Hegnerová K, Piliarik M, Sanchez-Baeza F, Homola J, Marco MP (2010) A label-free and portable multichannel surface plasmon resonance immunosensor for on site analysis of antibiotics in milk samples. Biosens Bioelectron 26(4):1231–1238CrossRefGoogle Scholar
  22. 22.
    Viswanathan S, Radecka H, Radecki J (2009) Electrochemical biosensors for food analysis. Monatsh Chem/Chem Mon 140(8):891–899CrossRefGoogle Scholar
  23. 23.
    Adrián J, Fernández F, Muriano A, Obregon R, Ramón-Azcon J, Tort N, Marco MP (2009) Biosensors for pharmaceuticals and emerging contaminants based on novel micro and nanotechnology approaches. In: Barceló D, Hansen P-D (eds) Biosensors for environmental monitoring of aquatic systems. Handbook of environmental chemistry, part 5J. Springer, Berlin, pp 47–68CrossRefGoogle Scholar
  24. 24.
    Adrian J, Pasche S, Voirin G, Adrian J, Pinacho DG, Font H, Sánchez-Baeza F, Marco MP, Diserens J-M, Granier B (2009) Wavelength-interrogated optical biosensor for multi-analyte screening of sulfonamide, fluoroquinolone, β-lactam and tetracycline antibiotics in milk. Trends Anal Chem 28(6):769–777CrossRefGoogle Scholar
  25. 25.
    Bratov A, Abramova N, Pilar Marco M, Sanchez-Baeza F (2012) Three-dimensional interdigitated electrode array as a tool for surface reactions registration. Electroanalysis 24(1):69–75. doi: 10.1002/elan.201100392 CrossRefGoogle Scholar
  26. 26.
    Fernandez F, Pinacho DG, Sanchez-Baeza F, Pilar Marco M (2011) Portable surface plasmon resonance immunosensor for the detection of fluoroquinolone antibiotic residues in milk. J Agric Food Chem 59(9):5036–5043. doi: 10.1021/jf1048035 CrossRefGoogle Scholar
  27. 27.
    Fernandez F, Sanchez-Baeza F, Pilar Marco M (2012) Nanogold probe enhanced surface plasmon resonance immunosensor for improved detection of antibiotic residues. Biosens Bioelectron 34(1):151–158. doi: 10.1016/j.bios.2012.01.036 CrossRefGoogle Scholar
  28. 28.
    Giroud F, Gorgy K, Gondran C, Cosnier S, Pinacho DG, Marco MP, Sanchez-Baeza FJ (2009) Impedimetric immunosensor based on a polypyrrole-antibiotic model film for the label-free picomolar detection of ciprofloxacin. Anal Chem 81(20):8405–8409. doi: 10.1021/ac901290m CrossRefGoogle Scholar
  29. 29.
    Muriano A, Anisha Thayil KN, Salvador JP, Loza-Alvarez P, Soria S, Galve R, Marco MP (2012) Two-photon fluorescent immunosensor for androgenic hormones using resonant grating waveguide structures. Sensors Actuators B Chem 174:394–401. doi: 10.1016/j.snb.2012.08.006 CrossRefGoogle Scholar
  30. 30.
    Jornet D, González-Martínez MA, Puchades R, Maquieira A (2010) Antibiotic immunosensing: determination of sulfathiazole in water and honey. Talanta 81(4–5):1585–1592CrossRefGoogle Scholar
  31. 31.
    Centi S, Stoica A, Laschi S, Mascini M (2010) Development of an electrochemical immunoassay based on the use of an eight-electrodes screen-printed array coupled with magnetic beads for the detection of antimicrobial sulfonamides in honey. Electroanalysis 22(16):1881–1888CrossRefGoogle Scholar
  32. 32.
    Cai M, Zhu L, Ding Y, Wang J, Li J, Du X (2012) Determination of sulfamethoxazole in foods based on CeO2/chitosan nanocomposite-modified electrodes. Mater Sci Eng C 32(8):2623–2627. doi: 10.1016/j.msec.2012.08.017 CrossRefGoogle Scholar
  33. 33.
    Baniukevic J, Hakki Boyaci I, Goktug Bozkurt A, Tamer U, Ramanavicius A, Ramanaviciene A (2013) Magnetic gold nanoparticles in SERS-based sandwich immunoassay for antigen detection by well oriented antibodies. Biosens Bioelectron 43:281–288. doi: 10.1016/j.bios.2012.12.014 CrossRefGoogle Scholar
  34. 34.
    Kuramitz H (2009) Magnetic microbead-based electrochemical immunoassays. Anal Bioanal Chem 394(1):61–69. doi: 10.1007/s00216-009-2650-y CrossRefGoogle Scholar
  35. 35.
    Orlov AV, Khodakova JA, Nikitin MP, Shepelyakovskaya AO, Brovko FA, Laman AG, Grishin EV, Nikitin PI (2013) Magnetic immunoassay for detection of staphylococcal toxins in complex media. Anal Chem 85(2):1154–1163. doi: 10.1021/ac303075b CrossRefGoogle Scholar
  36. 36.
    Pedrero M, Campuzano S, Pingarron JM (2012) Magnetic beads-based electrochemical sensors applied to the detection and quantification of bioterrorism/biohazard agents. Electroanalysis 24(3):470–482. doi: 10.1002/elan.201100528 CrossRefGoogle Scholar
  37. 37.
    Xu J, Yin W, Zhang Y, Yi J, Meng M, Wang Y, Xue H, Zhang T, Xi R (2012) Establishment of magnetic beads-based enzyme immunoassay for detection of chloramphenicol in milk. Food Chem 134(4):2526–2531. doi: 10.1016/j.foodchem.2012.04.083 CrossRefGoogle Scholar
  38. 38.
    Zacco E, Adrian J, Galve R, Marco M-P, Alegret S, Pividori MI (2007) Electrochemical magneto immunosensing of antibiotic residues in milk. Biosens Bioelectron 22(9–10):2184–2191CrossRefGoogle Scholar
  39. 39.
    Adrian J, Font H, Diserens J-M, Sanchez-Baeza F, Marco MP (2009) Generation of broad specificity antibodies for sulfonamide antibiotics and development of an enzyme-linked immunosorbent assay (ELISA) for the analysis of milk samples. J Agric Food Chem 57(2):385–394. doi: 10.1021/jf8027655 CrossRefGoogle Scholar
  40. 40.
    Font H, Adrian J, Galve R, Estevez MC, Castellari M, Gratacos-Cubarsí M, Sanchez-Baeza F, Marco MP (2008) Immunochemical assays for direct sulfonamide antibiotic detection in milk and hair samples using antibody derivatized magnetic nanoparticles. J Agric Food Chem 56(3):736–743. doi: 10.1021/jf072550n CrossRefGoogle Scholar
  41. 41.
    Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(1–2):248–254CrossRefGoogle Scholar
  42. 42.
    Zacco E, Pividori MI, Alegret S, Galve R, Marco M-P (2006) Electrochemical magnetoimmunosensing strategy for the detection of pesticides residues. Anal Chem 78(6):1780–1788CrossRefGoogle Scholar
  43. 43.
    Pividori MI, Merkoçi A, Alegret S (2003) Graphite-epoxy composites as a new transducing material for electrochemical genosensing. Biosens Bioelectron 19:473–484CrossRefGoogle Scholar
  44. 44.
    Lermo A, Fabiano S, Hernández S, Galve R, Marco MP, Alegret S, Pividori MI (2009) Immunoassay for folic acid detection in vitamin-fortified milk based on electrochemical magneto sensors. Biosens Bioelectron 24(7):2057–2063CrossRefGoogle Scholar
  45. 45.
    Adrian J, Pasche S, Diserens J-M, Sánchez-Baeza F, Gao H, Marco MP, Voirin G (2009) Waveguide interrogated optical immunosensor (WIOS) for detection of sulfonamide antibiotics in milk. Biosens Bioelectron 24(11):3340–3346CrossRefGoogle Scholar
  46. 46.
    Adrian J, Pinacho D, Granier B, Diserens J-M, Sánchez-Baeza F, Marco MP (2008) A multianalyte ELISA for immunochemical screening of sulfonamide, fluoroquinolone and ß-lactam antibiotics in milk samples using class-selective bioreceptors. Anal Bioanal Chem 391(5):1703–1712CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • A. Muriano
    • 1
    • 2
  • D.-G. Pinacho
    • 1
    • 2
  • V. Chabottaux
    • 3
  • J.-M. Diserens
    • 4
  • B. Granier
    • 3
  • S. Stead
    • 5
  • F. Sanchez Baeza
    • 1
    • 2
  • M. I. Pividori
    • 6
  • M.-P. Marco
    • 1
    • 2
  1. 1.Nanobiotechnology for Diagnostics Group (Nb4D), IQAC-CSICBarcelonaSpain
  2. 2.CIBER de Bioingeniería, Biotemateriales y Nanomedicina (CIBER-BBN)BarcelonaSpain
  3. 3.UnisensorWandreBelgium
  4. 4.Nestlé Research CenterLausanne 26Switzerland
  5. 5.Food and Environmental Research AgencyYorkUK
  6. 6.Sensors & Biosensors GroupAutonomous University of Barcelona (UAB)BellaterraSpain

Personalised recommendations