Metody stosowane do wykrywania i identyfikacji toksyn botulinowych w próbkach klinicznych i żywności*

REVIEW ARTICLE

Metody stosowane do wykrywania i identyfikacji toksyn botulinowych w próbkach klinicznych i żywności*

Karolina Rudnicka 1 , Karolina Durka 1 , Paweł Chwaluk 2 , Magdalena Chmiela 1

1. Pracownia Gastroimmunologii, Katedra Immunologii i Biologii Infekcyjnej, Wydział Biologii i Ochrony Środowiska, Uniwersytet Łódzki,
2. Wojewódzki Szpital Specjalistyczny w Białej Podlaskiej, Biała Podlaska,

Published: 2020-05-15
DOI: 10.5604/01.3001.0014.1439
GICID: 01.3001.0014.1439
Available language versions: en pl
Issue: Postepy Hig Med Dosw 2020; 74 : 116-130

 

Abstract

Botulism is a severe neuroparalytic illness, which affects the nervous system. It is caused by botulinum neurotoxins (BoNTs), produced by anaerobic gram-positive bacteria Clostridium botulinum. There are 7 serotypes of BoNT A-G, but BoNT A/B/D/E plays a major role in botulism affecting humans. Foodborne botulism (classic botulism) is the most frequent clinical manifestation occurring after consumption of food containing botulinum neurotoxins. The diagnosis of botulism is based on clinical symptoms; however, recommended and alternative laboratory methods are used to confirm the etiology of symptoms and the identification of BoNT toxin type. The aim of this work was to present the epidemiology of foodborne botulism in Poland and to gather and analyze the available diagnostic methods that allow us to detect BoNT in clinical samples. Using the epidemiological reports of National Institute of Hygiene in Poland and findings presented in the Przegląd Epidemiologiczny, the incidence of classical botulism in Poland has been presented over a period of recent 18 years. Searching for the optimal diagnostic method for BoNT identification in various samples, we have confronted the sensitivity and specificity of recently available alternative methods with classical biological assay.

References

  • 1. Advisory Committee on the Microbiological Safety of Food. 2006.Report on minimally proceessed infant weaning foods and the risk ofinfant botulism. https://acmsf.food.gov.uk/sites/default/files/mnt/drupal_data/sources/files/multimedia/pdfs/infantbotulismreport.pdf (28.08.2019)
    Google Scholar
  • 2. Angulo F.J., Getz J., Taylor J.P., Hendricks K.A., Hatheway C.L.,Barth S.S., Solomon H.M., Larson A.E., Johnson E.A., Nickey L.N., RiesA.A.: A large outbreak of botulism: the hazardous baked potato. J.Infect. Dis., 1998; 178: 172–177
    Google Scholar
  • 3. Artin I.: Real-time PCR for diagnosis of botulism and quantificationof neurotoxin gene expression in Clostridium botulinum. PhDthesis, Division of Medical Microbiology, Lund University, 2008
    Google Scholar
  • 4. Babrak L., Lin A., Stanker L.H., McGarvey J., Hnasko R.: Rapid microfluidicassay for the detection of botulinum neurotoxin in animalsera. Toxins, 2016; 8: 13
    Google Scholar
  • 5. Bagramyan K., Barash J.R., Arnon S.S., Kalkum M.: Attomolar detectionof botulinum toxin type A in complex biological matrices.PLoS One, 2008; 3: e2041
    Google Scholar
  • 6. Bagramyan K., Kalkum M.: Ultrasensitive detection of botulinumneurotoxins and anthrax lethal factor in biological samplesby ALISSA. Methods Mol. Biol., 2011; 739: 23-36
    Google Scholar
  • 7. Bahadır E.B., Sezgintürk M.K.: Lateral flow assays: Principles, designsand labels. Trends Anal. Chem., 2016; 82: 286–306
    Google Scholar
  • 8. Barash, J.R., Arnon, S.S.: A novel strain of Clostridium botulinumthat produces type B and type H botulinum toxins. J. Infect. Dis.2014; 209: 183–191
    Google Scholar
  • 9. Barr J.R., Moura H., Boyer A.E., Woolfitt A.R., Kalb S.R., PavlopoulosA., McWilliams L.G., Schmidt J.G., Martinez R.A., Ashley D.L.:Botulinum neurotoxin detection and differentiation by mass spectrometry.Emerg. Infect. Dis., 2005; 11: 1578–1583
    Google Scholar
  • 10. Basavanna U., Muruvanda T., Brown E.W., Sharma S.K.: Developmentof a cell-based functional assay for the detection of Clostridiumbotulinum neurotoxin types A and E. Int. J. Microbiol., 2013; 2013: 593219
    Google Scholar
  • 11. Bielec D., Modrzewska R.: Zatrucie jadem kiełbasianym dawnieji dziś – aspekty kliniczne. Przegl. Epidemiol., 2007; 61: 505–512
    Google Scholar
  • 12. Bielec D., Semczuk G., Lis J., Firych J., Modrzewska R., JanowskiR.: Epidemiologia i klinika zatruć jadem kiełbasianym chorych leczonychw Klinice Chorób Zakaźnych Akademii Medycznej w Lubliniew latach 1990–2000. Przegl. Epidemiol., 2002; 56: 435–442
    Google Scholar
  • 13. Čapek P., Dickerson T.J.: Sensing the deadliest toxin: Technologiesfor botulinum neurotoxin detection. Toxins, 2010; 2: 24–53
    Google Scholar
  • 14. Carter A.T., Peck M.W.: Genomes, neurotoxins and biology of Clostridiumbotulinum group I and group II. Res Microbiol., 2015; 166: 303–317
    Google Scholar
  • 15. Center for Food Safety and Applied Nutrition (CFSAN). BacteriologicalAnalytical Manual, U.S. Food and Drug Administration,Washington, 2011
    Google Scholar
  • 16. Centers for Disease Control and Prevention: Botulism in theUnited States, 1899–1996 Handbook for Epidemiologists, Clinicians,and Laboratory Workers. Department of Health and Human Services,CDC, Atlanta, 1998
    Google Scholar
  • 17. Chao H.Y., Wang Y.C., Tang S.S., Liu H.W.: A highly sensitiveimmune-polymerase chain reaction assay for Clostridium botulinumneurotoxin type A. Toxicon, 2004; 43: 27–34
    Google Scholar
  • 18. Cheng L.W., Henderson T.D.2nd: Comparison of oral toxicologicalproperties of botulinum neurotoxin serotypes A and B. Toxicon,2011; 58: 62–67
    Google Scholar
  • 19. Cheng L.W., Land K.M., Stanker L.H.: Current methods for detectingthe presence of botulinum neurotoxins in food and other biological samples.W: Bioterrorism, red.: S.A. Morse, InTechOpen, London 201: 1–16
    Google Scholar
  • 20. Cheng L.W., Land K.M., Tam C., Brandon D.L., Stanker L.H.: Technologiesfor detecting botulinum neurotoxins in biological and environmentalmatrices. W: Significance, Prevention and Control of FoodRelated Diseases, red.: H. Makun. InTechOpen, London 2016, 125–144
    Google Scholar
  • 21. Cheng L.W., Onisko B., Johnson E.A., Reader J.R., Griffey S.M.,Larson A.E., Tepp W.H., Stanker L.H., Brandon D.L., Carter J.M.: Effectsof purification on the bioavailability of botulinum neurotoxintype A. Toxicology, 2008; 249: 123–129
    Google Scholar
  • 22. Chiao D.J., Shyu R.H., Hu C.S., Chiang H.Y., Tang S.S.: Colloidalgold-based immunochromatographic assay for detection of botulinumneurotoxin type B. J. Chromatogr. B: Anal. Technol. Biomed.Life Sci., 2004; 809: 37–41
    Google Scholar
  • 23. Choroby zakaźne i zatrucia w Polsce (biuletyn roczny). http://wwwold.pzh.gov.pl/oldpage/epimeld/index_p.html (15.05.2018)
    Google Scholar
  • 24. Christian T., Suryadi K., Shine N.: Ultra Sensitive HPLC DetectionAssay for Botulinum Neurotoxin Type A. Presented at the 47thAnnual Interagency Botulinum Research Coordinating CommitteeMeeting, Atlanta, 2010
    Google Scholar
  • 25. Chwaluk P., Chwaluk A.: Trudności diagnostyczne w zatruciujadem kiełbasianym – opis przypadków i przegląd piśmiennictwa.Przegl. Lek., 2007; 64: 348–351
    Google Scholar
  • 26. Czerwiński M., Czarkowski M.P., Kondej B.: Zatrucia jadem kiełbasianymw Polsce w 2007 roku. Przegl. Epidemiol., 2009; 63: 237–240
    Google Scholar
  • 27. Czerwiński M., Czarkowski M.P., Kondej B.: Zatrucia jadem kiełbasianymw Polsce w 2008 roku. Przegl. Epidemiol., 2010; 64: 231–234
    Google Scholar
  • 28. Czerwiński M., Czarkowski M.P., Kondej B.: Zatrucia jadem kiełbasianymw Polsce w 2009 roku. Przegl. Epidemiol., 2011; 65: 251–254
    Google Scholar
  • 29. Czerwiński M., Czarkowski M.P., Kondej B.: Zatrucia jadem kiełbasianymw Polsce w 2010 roku. Przegl. Epidemiol., 2012; 66: 267–271
    Google Scholar
  • 30. Czerwiński M., Czarkowski M.P., Kondej B.: Zatrucia jadem kiełbasianymw Polsce w 2011 roku. Przegl. Epidemiol., 2013; 67: 343–345
    Google Scholar
  • 31. Czerwiński M., Czarkowski M.P., Kondej B.: Zatrucia jadem kiełbasianymw Polsce w 2012 roku. Przegl. Epidemiol., 2014; 68: 357–359
    Google Scholar
  • 32. Czerwiński M., Czarkowski M.P., Kondej B.: Zatrucia jadem kiełbasianymw Polsce w 2013 roku. Przegl. Epidemiol., 2015; 69: 363–365
    Google Scholar
  • 33. Czerwiński M., Czarkowski M.P., Kondej B.: Zatrucia jadem kiełbasianymw Polsce w 2014 roku. Przegl. Epidemiol., 2016; 70: 217–223
    Google Scholar
  • 34. Czerwiński M., Czarkowski M.P., Kondej B.: Zatrucia jadem kiełbasianymw Polsce w 2015 roku. Przegl. Epidemiol., 2017; 71: 339–344
    Google Scholar
  • 35. Definicje przypadków chorób zakaźnych na potrzeby nadzoruepidemiologicznego. http://wwwold.pzh.gov.pl/oldpage/epimeld/inne/Def_PL2_4.pdf (27.03.2018)
    Google Scholar
  • 36. Dong M., Tepp W.H., Johnson E.A., Chapman E.R.: Using fluorescentsensors to detect botulinum neurotoxin activity in vitro and inliving cells. Proc. Natl Acad. Sci. USA, 2004; 101: 14701–14706
    Google Scholar
  • 37. Dorner M. B, Schulz K.M., Kull S., Dorner B.G.: Complexity ofbotulinum neurotoxin: Challenges for detection technology. Curr.Top. Microbiol. Immunol., 2013; 364: 219–255
    Google Scholar
  • 38. Drożdżyńska M., Sobieraj-Garbiak I., Chlasta A., Jastrzębska M.:Toksyna botulinowa i jej zastosowanie w medycynie. Diagn. Lab.,2015; 51: 139–146
    Google Scholar
  • 39. Dunning F.M., Piazza T.M., Zeytin F.N., Tucker W.C.: Isolationand quantification of botulinum neurotoxin from complex matricesusing the BoTest matrix assays. J. Vis. Exp., 2014; 2014: e51170
    Google Scholar
  • 40. Eckle V.S., Drexler B., Grasshoff C., Seeger T., Thiermann H., AntkowiakB.: Spinal cord – skeletal muscle cocultures detect musclerelaxantaction of botulinum neurotoxin A. ALTEX, 2014; 31: 433–440
    Google Scholar
  • 41. Fan Y., Barash J.R., Lou J., Conrad F., Marks J.D., Arnon, S.S.: Immunologicalcharacterization and neutralizing ability of monoclonalantibodies directed against botulinum neurotoxin type H. J. Infect.Dis., 2016; 213: 1606–1614
    Google Scholar
  • 42. Fenicia L., Anniballi F., De Medici D., Delibato E., Aureli P.: SYBRGreen real-time PCR method to detect Clostridium botulinum type A.Appl. Environ. Microbiol., 2007; 73: 2891–2896
    Google Scholar
  • 43. Fernández-Salas E., Wang J., Molina Y., Nelson J.B., JackyB.P.S., Aoki K.R.: Botulinum neurotoxin serotype a specific cellbasedpotency assay to replace the mouse bioassay. PLoS One,2012; 7: e49516
    Google Scholar
  • 44. Ferreira J.L., Eliasberg S.J., Edmonds P., Harrison M.A.: Comparisonof the mouse bioassay and enzyme-linked immunosorbent assayprocedures for the detection of type A botulinal toxin in food.J. Food Prot., 2004; 67: 203–206
    Google Scholar
  • 45. Gessler F., Pagel Wieder S., Avondet M.A., Böhnel H.: Evaluationof lateral flow assays for the detection of botulinum neurotoxin typeA and their application in laboratory diagnosis of botulism. Diagn.Microbiol. Infect. Dis., 2007; 57: 243–249
    Google Scholar
  • 46. Grate J.W., Ozanich R.M., Jr., Warner M.G., Bruckner-Lea C.J.,Marks J.D.: Advances in assays and analytical approaches for botulinum-toxin detection. Trends Anal. Chem., 2010; 29: 1137–1156
    Google Scholar
  • 47. Grenda T., Kukier E., Kwiatek K.: Methods and difficulties indetection of Clostridium botulinum and its toxins. Pol. J. Vet. Sci.,2014; 17: 195–205
    Google Scholar
  • 48. Grygorczuk S., Pancewicz S., Kondrusik M., Zajkowska J.: Zatrucietoksyną botulinową – trudności diagnostyczne. Pol. Merk.Lek., 2000; 50: 572
    Google Scholar
  • 49. Guglielmo-Viret V., Attrée O., Blanco-Gros V., Thullier P.: Comparisonof electrochemiluminescence assay and ELISA for the detectionof Clostridium botulinum type B neurotoxin. J. Immunol. Methods,2005; 301: 164–172
    Google Scholar
  • 50. Guo J., Xu C., Li X., Chen S.: A simple, rapid and sensitive FRETassay for botulinum neurotoxin serotype B detection. PLoS One,2014; 9: e114124
    Google Scholar
  • 51. Halliwell J., Gwenin C.: A label free colorimetric assay for thedetection of active botulinum neurotoxin type A by SNAP-25 conjugatedcolloidal gold. Toxins, 2013; 5: 1381–1391
    Google Scholar
  • 52. Hill K.K., Smith T.J., Helma C.H., Ticknor L.O., Foley B.T., SvenssonR.T., Brown J.L., Johnson E.A., Smith L.A., Okinaka R.T., JacksonP.J., Marks J.D.: Genetic diversity among botulinum neurotoxin-producingclostridial strains. J. Bacteriol., 2007; 189: 818–832
    Google Scholar
  • 53. Hobbs R.J., Thomas C.A., Halliwell J., Gwenin C.D.: Rapid detectionof botulinum neurotoxins – a review. Toxins, 2019; 11: 418
    Google Scholar
  • 54. Hörman A., Nevas M., Lindström M., Hänninen M.L., KorkealaH.: Elimination of botulinum neurotoxin (BoNT) type B from drinkingwater by small-scale (personal-use) water purification devicesand detection of BoNT in water samples. Appl. Environ. Microbiol.,2005; 71: 1941–1945
    Google Scholar
  • 55. Interagency Coordinating Committee on the Validation of AlternativeMethods (ICCVAM), National Toxicology Program InteragencyCenter for the Evaluation of Alternative Toxicological Methods (NICEATM):Report on the ICCVAM-NICEATM/ECVAM Scientific Workshopon Alternative Methods to Refine, Reduce or Replace the MouseLD50 Assay for Botulinum Toxin Testing. NIH Publication 08-6416
    Google Scholar
  • 56. Jones R.G., Marks J.D.: Use of a new functional dual coating (FDC)assay to measure low toxin levels in serum and food samples followingan outbreak of human botulism. J. Med. Microbiol., 2013; 62: 828–835
    Google Scholar
  • 57. Jones R.G., Ochiai M., Liu Y., Ekong T., Sesardic D.: Developmentof improved SNAP25 endopeptidase immuno-assays for botulinumtype A and E toxins. J. Immunol. Methods, 2008; 329: 92–101
    Google Scholar
  • 58. Kalb S.R., Baudys J., Wang D., Barr J.R.: Recommended massspectrometry-based strategies to identify botulinum neurotoxin–containing samples. Toxins, 2015; 7: 1765–1778
    Google Scholar
  • 59. Kalb S.R., Garcia-Rodriguez C., Lou J., Baudys J., Smith T.J., MarksJ.D., Smith L.A., Pirkle J.L., Barr J.R.: Extraction of BoNT/A,/B,/E, and/F with a single, high affinity monoclonal antibody for detectionof botulinum neurotoxin by Endopep-MS. PLoS One, 2010; 5: e12237
    Google Scholar
  • 60. Kalb S.R., Goodnough M.C., Malizio C.J., Pirkle J.L., Barr J.R.:Detection of botulinum neurotoxin A in a spiked milk sample withsubtype identification through toxin proteomics. Anal. Chem., 2005;77: 6140–6146
    Google Scholar
  • 61. Kalb S.R., Moura H., Boyer A.E., McWilliams L.G., Pirkle J.L., BarrJ.R.: The use of Endopep-MS for the detection of botulinum toxins A, B,E, and F in serum and stool samples. Anal. Biochem., 2006; 351: 84–92
    Google Scholar
  • 62. Kalb S.R., Santana W.I., Pirkle J.L., Barr J.R.: Detection, differentiation,and subtyping of botulinum toxins A, B, E, and F by massspectrometry. Botulinum J., 2012; 2: 119–134
    Google Scholar
  • 63. Kizerwetter-Świda M., Binek M.: Zatrucie jadem kiełbasianym –problem wciąż aktualny. Post. Mikrobiol., 2010; 49: 75–85
    Google Scholar
  • 64. Koh C.Y., Schaff U.Y., Piccini M.E., Stanker L.H., Cheng L.W.,Ravichandran E., Singh B.R., Sommer G.J., Singh A.K.: Centrifugal microfluidicplatform for ultrasensitive detection of botulinum toxin.Anal. Chem., 2015; 87: 922–928
    Google Scholar
  • 65. Kolesnikov A.V., Kozyr A.V., Ryabko A.K., Shemyakin I.G.: Ultrasensitivedetection of protease activity of anthrax and botulinumtoxins by a new PCR-based assay. Pathog. Dis., 2016; 74: 112
    Google Scholar
  • 66. Kukier E., Kwiatek K., Grenda T., Goldsztejn M., Dębski J.: Botulizm– patogeneza i diagnostyka choroby. Życie Wet., 2015; 90: 163–166
    Google Scholar
  • 67. Kukier E., Goldsztejn M., Kozieł N., Kwiatek K. Zacharczuk K.:Clostridium botulinum i toksyny botulinowe. Potencjalne zagrożeniew mleku i produktach mlecznych. Przem. Spoż., 2017; 71: 28–33
    Google Scholar
  • 68. Liu J., Gao S., Kang L., Ji B., Xin W., Kang J., Li P., Gao J., Wang H.,Wang J., Yang H.: An ultrasensitive gold nanoparticle-based lateralflow test for the detection of active botulinum neurotoxin type A.Nanoscale Res. Lett., 2017; 12: 227
    Google Scholar
  • 69. Loutfy M.R., Austin J.W., Blanchfield B., Fong I.W.: An outbreakof foodborne botulism in Ontario. Can J. Infect. Dis., 2003 14: 206–209
    Google Scholar
  • 70. Markey B., Leonard F., Archambault M., Cullinane A., Maguire D.:Clinical Veterinary Microbiology. Mosby Elsevier, Philadelphia 2013
    Google Scholar
  • 71. Maslanka S.E., Lúquez C., Dykes J.K., Tepp W.H., Pier C.L., PellettS., Raphael B.H., Kalb S.R., Barr J.R., Rao A., Johnson E.A.: A novelbotulinum neurotoxin, previously reported as serotype H, hasa hybrid-like structure with regions of similarity to the structuresof serotypes A and F and is neutralized with serotype A antitoxin. J.Infect. Dis., 2016; 213: 379–385
    Google Scholar
  • 72. Maslanka S.E., Luquez C., Raphael H.B., Dykes J.K., Joseph L.A.:Utility of botulinum toxin ELISA A, B, E, F kits for clinical laboratoryinvestigation of human botulism. Botulinum J., 2011; 2: 72–92
    Google Scholar
  • 73. Merz Pharma GmbH, landmark change for botulinum neurotoxin:alternative test method approved in the U.S. https://www.merz.com/Ablog/news/botulinum-neurotoxin/(24.08.2019)
    Google Scholar
  • 74. Nantel A.J.: Clostridium botulinum – International programme onchemical safety poisons information monograph (858 Bacteria). http://www.who.int/csr/delibepidemics/clostridiumbotulism.pdf (10.04.2018)
    Google Scholar
  • 75. NCFA, Nordic Committee on Food Analysis. 1991. Botulinumtoxin. Detection in foods, blood, and other materials. NCFA methodno 80 2nd ed. Espoo, Finland
    Google Scholar
  • 76. Nevas M.: Clostridium botulinum in honey production with respectto infant botulism. Doctoral dissertation. University of Helsinki.Helsinki, 2006
    Google Scholar
  • 77. Niemeyer C.M., Adler M., Wacker R.: Immuno-PCR: high sensitivitydetection of proteins by nucleic acid amplification. TrendsBiotechnol., 2005; 23: 208–216
    Google Scholar
  • 78. Ohishi I., Sakaguchi G.: Oral toxicities of Clostridium botulinumtype C and D toxins of different molecular sizes. Infect. Immun.,1980; 28: 303–309
    Google Scholar
  • 79. Peck M.W., Smith T.J., Anniballi F., Austin J.W., Bano L., BradshawM., Cuervo P., Cheng L.W., Derman Y., Dorner B.G., Fisher A., Hill K.K.,Kalb S.R., Korkeala H., Lindström M. i wsp.: Historical perspectivesand guidelines for botulinum neurotoxin subtype nomenclature.Toxins, 2017; 9: 38
    Google Scholar
  • 80. Pellett S., Tepp W.H., Johnson E.A., Sesardic D.: Assessment ofELISA as endpoint in neuronal cell-based assay for BoNT detectionusing hiPSC derived neurons. J. Pharmacol. Toxicol. Methods,2017; 88: 1–6
    Google Scholar
  • 81. Pellett S., Tepp W.H., Toth S.I., Johnson E.A.: Comparison of theprimary rat spinal cord cell (RSC) assay and the mouse bioassay forbotulinum neurotoxin type A potency determination. J. Pharmacol.Toxicol. Methods, 2010; 61: 304–310
    Google Scholar
  • 82. Perry M.J., Centurioni D.A., Davis S.W., Hannett G.E., MusserK.A., Egan C.T.: Implementing the Bruker MALDI Biotyper in thePublic Health Laboratory for C. botulinum neurotoxin detection. Toxins,2017; 9: 94
    Google Scholar
  • 83. Pires-Alves M., Ho M., Aberle K.K., Janda K.D., Wilson B.A.: Tandemfluorescent proteins as enhanced FRET-based substrates forbotulinum neurotoxin activity. Toxicon, 2009; 53: 392–399
    Google Scholar
  • 84. Rasetti-Escargueil C., Jones R.G., Liu Y., Sesardic D.: Measurementof botulinum types A, B and E neurotoxicity using the phrenicnerve-hemidiaphragm: improved precision with in-bred mice. Toxicon,2009; 53: 503–511
    Google Scholar
  • 85. Rivera V.R., Gamez F.J., Keener W.K., White J.A., Poli M.A.: Rapiddetection of Clostridium botulinum toxins A, B, E, and F in clinicalsamples, selected food matrices, and buffer using paramagneticbead-based electrochemiluminescence detection. Anal. Biochem.,2006; 353: 248–256
    Google Scholar
  • 86. Rudnicka K., Kwiatkowska P., Gajewski A., Chmiela M.: Mikrofloramiodu jako źródło spor C. botulinum i przyczyna rozwoju botulizmuniemowląt – rozważania na temat zasadności oczyszczaniamiodu w kontekście obowiązującego prawa. Post. Mikrobiol., 2015;54: 184–194
    Google Scholar
  • 87. Rudnicka K., Tenderenda M., Chmiela M.: Etiologia i epidemiologiabotulizmu niemowląt. Ped. Pol., 2014; 89: 198–202
    Google Scholar
  • 88. Rust A., Doran C., Hart R., Binz T., Stickings P., Sesardic D., PedenA.A., Davletov B.: A cell line for detection of botulinum neurotoxintype B. Front. Pharmacol., 2017; 8: 796
    Google Scholar
  • 89. Sarita R., Ponmariappan S., Sharma A., Kamboj D.V., Jain A.K.:Development of immunodetection system for botulinum neurotoxinserotype E. Indian J. Med. Res., 2018; 147: 603–610
    Google Scholar
  • 90. Scarlatos A., Welt B.A., Cooper B.Y., Archer D., DeMarse T., ChauK.V.: Methods for detecting botulinum toxin with applicability toscreening foods against biological terrorist attacks. J. Food Sci., 2005;70: 121–130
    Google Scholar
  • 91. Schantz E.J., Kautter D.A.: Standardized assay for Clostridiumbotulinum toxins. J. AOAC Int., 1978; 61: 96–99
    Google Scholar
  • 92. Schmidt J.J., Stafford R.G., Millard C.B.: High-throughput assaysfor botulinum neurotoxin proteolytic activity: serotypes A, B, D, andF. Anal. Biochem., 2001; 296: 130–137
    Google Scholar
  • 93. Shapiro R.L., Hatheway C., Becher J., Swerdlow D.L.: Botulismsurveillance and emergency response: a public health strategy fora global challenge. JAMA, 1997; 278: 433–435
    Google Scholar
  • 94. Sharma S.K., Eblen B.S., Bull R.L., Burr D.H., Whiting R.C.: Evaluationof lateral-flow Clostridium botulinum neurotoxin detection kitsfor food analysis. Appl. Environ. Microbiol., 2005; 71: 3935–3941
    Google Scholar
  • 95. Sharma S.K., Ferreira J.L., Eblen B.S., Whiting R.C.: Detection oftype A, B, E, and F Clostridium botulinum neurotoxins in foods by usingan amplified enzyme-linked immunosorbent assay with digoxigeninlabeledantibodies. Appl. Environ. Microbiol., 2006; 72: 1231–1238
    Google Scholar
  • 96. Sharma S.K., Whiting R.C.: Methods for detection of Clostridiumbotulinum toxin in foods. J. Food Prot., 2005; 68: 1256–1263
    Google Scholar
  • 97. Singh A.K., Stanker L.H., Sharma S.K.: Botulinum neurotoxin:where are we with detection technologies? Crit. Rev. Microbiol.,2013; 39: 43–56
    Google Scholar
  • 98. Śliwińska-Mossoń M., Małolepsza K.: Diagnostyka i leczeniezatruć toksyną botulinową. Fam. Med. Prim. Care Rev., 2011; 13: 68–73
    Google Scholar
  • 99. Smith T.J., Lou J., Geren I.N., Forsyth C.M., Tsai R., Laporte S.L.,Tepp W.H., Bradshaw M., Johnson E.A., Smith L.A., Marks J.D.: Sequencevariation within botulinum neurotoxin serotypes impacts antibodybinding and neutralization. Infect. Immun., 2005; 73: 5450–5457
    Google Scholar
  • 100. Stanker L.H., Merrill P., Scotcher M.C., Cheng L.W.: Developmentand partial characterization of high-affinity monoclonal antibodiesfor botulinum toxin type A and their use in analysis of milk by sandwichELISA. J. Immunol. Methods, 2008; 336: 1–8
    Google Scholar
  • 101. Stanker L.H., Scotcher M.C., Cheng L., Ching K., McGarvey J.,Hodge D., Hnasko R.: A monoclonal antibody based capture ELISAfor botulinum neurotoxin serotype B: toxin detection in food. Toxins,2013; 5: 2212–2226
    Google Scholar
  • 102. Stern D., von Berg L., Skiba M., Dorner M.B., Dorner B.G.: Replacingthe mouse bioassay for diagnostics and potential testingof botulinum neurotoxins – progress and challenges. Berl. Münch.Tierärztl. Wochenschr., 2018; 131: 375–394
    Google Scholar
  • 103. Taylor K., Gericke C., Alvarez L.R.: Botulinum toxin testing onanimals is still a Europe-wide issue. ALTEX, 2019; 36: 81–90
    Google Scholar
  • 104. Thirunavukkarasu N., Johnson E., Pillai S., Hodge D., StankerL., Wentz T., Singh B., Venkateswaran K., McNutt P., Adler M., BrownE., Hammack T., Burr D., Sharma S.: Botulinum neurotoxin detectionmethods for Public Health Response and surveillance. Front. Bioeng.Biotechnol., 2018; 6: 80
    Google Scholar
  • 105. Truant A.L., Tang Y.W., Waites K.B., Bébéar C., Rennie R.P.: Manualof Commercial Methods in Clinical Microbiology: InternationalEdition, 2nd Edition. John Wiley & Sons, Hoboken 2016
    Google Scholar
  • 106. Wang D., Baudys J., Kalb S.R., Barr J.R.: Improved detection ofbotulinum neurotoxin type A in stool by mass spectrometry. Anal.Biochem., 2011; 412: 67–73
    Google Scholar
  • 107. Wang D., Baudys J., Ye Y., Rees J.C., Barr J.R., Pirkle J.L., KalbS.R.: Improved detection of botulinum neurotoxin serotype A byEndopep-MS through peptide substrate modification. Anal. Biochem.,2013; 432: 115–123
    Google Scholar
  • 108. Wang D., Krilich J., Baudys J., Barr J.R., Kalb S.R.: Optimizationof peptide substrates for botulinum neurotoxin E improves detectionsensitivity in the Endopep–MS assay. Anal. Biochem., 2015; 468: 15–21
    Google Scholar
  • 109. Wenham T., Cohen A.: Botulism. Continuing education in anaesthesia.Crit. Care Pain, 2008; 8: 21–25
    Google Scholar
  • 110. Wictome M., Newton K., Jameson K., Hallis B., Dunnigan P.,Mackay E., Clarke S., Taylor R., Gaze J., Foster K., Shone C.: Developmentof an in vitro bioassay for Clostridium botulinum type B neurotoxinin foods that is more sensitive than the mouse bioassay. Appl.Environ. Microbiol., 1999; 65: 3787–3792
    Google Scholar
  • 111. Wilder-Kofie T.D., Lúquez C., Adler M., Dykes J., Coleman J.K.,Coleman J.D., Maslanka S.E.: An alternative in vivo method to refinethe mouse bioassay for botulinum toxin detection. Comp. Med.,2011; 61: 235–242
    Google Scholar
  • 112. Yadirgi G., Stickings P., Rajagopal S., Liu Y., Sesardic D.: Immuno-detection of cleaved SNAP-25 from differentiated mouse embryonicstem cells provides a sensitive assay for determination ofbotulinum A toxin and antitoxin potency. J. Immunol. Methods,2017; 451: 90–99
    Google Scholar

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