Quantification of pyrrolizidine alkaloids in Senecio brasiliensis, beehive pollen, and honey by LC-MS/MS

References

• Erdős, N. Report on Prospects and Challenges for the EU Apiculture Sector; 2017/2115(INI), 2018.
   Google Scholar
• Giulietti, A. M.; Harley, R. M.; De Queiroz, L. P.; Wanderley, M. D. G. L.; Van Den Berg, C. Biodiversity and Conservation of Plants in Brazil. Conserv. Biol. 2005, 19, 632–639. DOI: 10.1111/j.1523-1739.2005.00704.x.
   Web of Science ®Google Scholar
• Silva, C. M.; Bolzan, A. A.; Heinzmann, B. M. Alcalóides Pirrolizidínicos Em Espécies Do Gênero Senecio. Quím. Nova 2006, 29, 1047–1053. DOI: 10.1590/S0100-40422006000500026.
   Google Scholar
• Stanski, C.; Moro, R. S. S.; Nogueira, M. K. F.; Kuniyoshi, Y. S.; da Luz, C. F. P. Palynology of Species of Anthemideae, Eupatorieae, Inuleae, Mutiseae and Senecianeae Tribes Occurring in the Region of Campos Gerais, Paraná State. Iheringia. Ser. Bot. 2018, 73, 353–362. DOI: 10.21826/2446-8231201873312.
   Web of Science ®Google Scholar
• Stegelmeier, B. L. Pyrrolizidine Alkaloid-Containing Toxic Plants (Senecio, Crotalaria, Cynoglossum, Amsinckia, Heliotropium, and Echium Spp.). Vet. Clin. N. Am. Food Anim. Pract. 2011, 27, 419–428. DOI: 10.1016/j.cvfa.2011.02.013.
   PubMed Web of Science ®Google Scholar
• Tokarnia, C. H.; Döbereiner, J. Plantas Tóxicas Do Brasil; Helianthus: Rio de Jnaeiro, 2000.
   Google Scholar
• Kast, C.; Kilchenmann, V.; Reinhard, H.; Droz, B.; Lucchetti, M. A.; Dübecke, A.; Beckh, G.; Zoller, O. Chemical Fingerprinting Identifies Echium vulgare, Eupatorium cannabinum and Senecio spp. as Plant Species Mainly Responsible for Pyrrolizidine Alkaloids in Bee-Collected Pollen. Food Addit. Contam. Part A 2018, 35, 316–327. DOI: 10.1080/19440049.2017.1378443.
   PubMed Web of Science ®Google Scholar
• Jesus, M. C.; Hungerford, N. L.; Carter, S. J.; Anuj, S. R.; Blanchfield, J. T.; De Voss, J. J.; Fletcher, M. T. Pyrrolizidine Alkaloids of Blue Heliotrope (Heliotropium Amplexicaule) and Their Presence in Australian Honey. J. Agric. Food Chem. 2019, 67, 7995–8006. DOI: 10.1021/acs.jafc.9b02136.
   PubMed Web of Science ®Google Scholar
• Colegate, S. M.; Upton, R.; Gardner, D. R.; Panter, K. E.; Betz, J. M. Potentially Toxic Pyrrolizidine Alkaloids in Eupatorium Perfoliatum and Three Related Species. Implications for Herbal Use as Boneset. Phytochem. Anal. 2018, 29, 613–626. DOI: 10.1002/pca.2775.
   PubMed Web of Science ®Google Scholar
• EFSA. Scientific Opinion on Pyrrolizidine Alkaloids in Food and Feed. EFSA J. 2011, 9, 2406. DOI: 10.2903/j.efsa..
   Google Scholar
• EFSA Panel on Contaminants in the Food Chain (CONTAM); Knutsen, H. K.; Alexander, J.; Barregård, L.; Bignami, M.; Brüschweiler, B.; Ceccatelli, S.; Cottrill, B.; Dinovi, M. Risks for Human Health Related to the Presence of Pyrrolizidine Alkaloids in Honey, Tea, Herbal Infusions and Food Supplements. EFSA J. 2017, 15, e04908. DOI: 10.2903/j.efsa.2017.4908.
   PubMed Web of Science ®Google Scholar
• Brugnerotto, P.; Seraglio, S. K. T.; Schulz, M.; Gonzaga, L. V.; Fett, R.; Costa, A. C. O. Pyrrolizidine Alkaloids and Beehive Products: A Review. Food Chem. 2021, 342, 128384. DOI: 10.1016/j.foodchem.2020.128384.
   PubMed Web of Science ®Google Scholar
• Mulder, P. P. J.; Sánchez, P. L.; These, A.; Preiss‐Weigert, A.; Castellari, M. Occurrence of Pyrrolizidine Alkaloids in Food. EFSA Support. Publ 2015, 12, 859E. DOI: 10.2903/sp.efsa.2015.en-859.
   Google Scholar
• Inacio, L. D. J.; Merlanti, R.; Lucatello, L.; Bisutti, V.; Contiero, B.; Serva, L.; Segato, S.; Capolongo, F. Pyrrolizidine Alkaloids in Bee Pollen Identified by LC-MS/MS Analysis and Colour Parameters Using Multivariate Class Modeling. Heliyon 2020, 6, e03593. DOI: 10.1016/j.heliyon.2020.e03593.
   PubMed Web of Science ®Google Scholar
• Kopp, T.; Abdel-Tawab, M.; Mizaikoff, B. Extracting and Analyzing Pyrrolizidine Alkaloids in Medicinal Plants: A Review. Toxins 2020, 12, 310–320. DOI: 10.3390/toxins12050320.
   PubMed Web of Science ®Google Scholar
• Valese, A. C.; Molognoni, L.; Ploêncio, L. A.; de S.; De Lima, F. G.; Gonzaga, L.; Górniak, S. L.; Daguer, H.; Barreto, F.; Carolina, A.; Costa, O. A Fast and Simple LC-ESI-MS/MS Method for Detecting Pyrrolizidine Alkaloids in Honey with Full Validation and Measurement Uncertainty. Food Control 2016, 67, 183–191. DOI: 10.1016/j.foodcont.2016.02.050.
   Web of Science ®Google Scholar
• Stuessy, T. F. Plant Taxonomy: The Systematic Evaluation of Comparative Data, Columbia University Press: New York, Second edition, 2009.
   Google Scholar
• Maurizio, A.; Louveaux, J. Pollens de Plantes Melliféres D’Europe; Paris: Union des Groupements Apicoles Francais, 1965.
   Google Scholar
• Barth, O. M. O Pólen No Mel Brasileiro; Rio de Janeiro: Gráfica Luxor, 1989.
   Google Scholar
• Barth, O. M. Análise Microscópica de Algumas Amostras de Mel. 1. Pólen Dominante. An. Acad. Bras. Cienc. 1970, 42, 351–366.
   Google Scholar
• Barth, O. M. Análise Microscópica de Algumas Amostras de Mel. 2. Pólen Acessório. An. Acad. Bras. Cienc. 1970, 42, 571–590.
   Google Scholar
• Barth, O. M. Análise Microscópica de Algumas Amostras de Mel. 3. Pólen Isolado. An. Acad. Bras. Cienc. 1970, 42, 747–772.
   Google Scholar
• Barth, O. M. Análise Microscópica de Algumas Amostras de Mel. 4. Espectro Polínico de Algumas Amostras de Mel Do Estado Do Rio De Janeiro. Rev. Bras. Biol. 1970, 30, 575–582.
   Google Scholar
• Barth, O. M. Análise Microscópica de Algumas Amostras de Mel. 5. Melato (“Honeydew”) Em Mel de Abelhas. Rev. Bras. Biol. 1970, 30, 601–608.
   Google Scholar
• Barth, O. M. Pollen, in Monofloral Honeys from Brazil. J. Apic. Res. 1990, 29, 89–94. DOI: 10.1080/00218839.1990.11101202.
   Web of Science ®Google Scholar
• Bezerra, M. A.; Ferreira, S. L. C.; Novaes, C. G.; dos Santos, A. M. P.; Valasques, G. S.; da Mata Cerqueira, U. M. F.; dos Santos Alves, J. P. Simultaneous Optimization of Multiple Responses and Its Application in Analytical Chemistry—A Review. Talanta 2019, 194, 941–959. DOI: 10.1016/j.talanta.2018.10.088.
   PubMed Web of Science ®Google Scholar
• Bezerra, M. A.; Santelli, R. E.; Oliveira, E. P.; Villar, L. S.; Escaleira, L. A. Response Surface Methodology (RSM) as a Tool for Optimization in Analytical Chemistry. Talanta 2008, 76, 965–977. DOI: 10.1016/j.talanta.2008.05.019.
   PubMed Web of Science ®Google Scholar
• Avula, B.; Sagi, S.; Wang, Y. H.; Zweigenbaum, J.; Wang, M.; Khan, I. A. Characterization and Screening of Pyrrolizidine Alkaloids and N-Oxides from Botanicals and Dietary Supplements Using UHPLC-High Resolution Mass Spectrometry. Food Chem. 2015, 178, 136–148. DOI: 10.1016/j.foodchem.2015.01.053.
   PubMed Web of Science ®Google Scholar
• Shimshoni, J. A.; Duebecke, A.; Mulder, P. P. J.; Cuneah, O.; Barel, S. Pyrrolizidine and Tropane Alkaloids in Teas and the Herbal Teas Peppermint, Rooibos and Chamomile in the Israeli Market. Food Addit. Contam. Part A 2015, 32, 2058–2067. DOI: 10.1080/19440049.2015.1087651.
   PubMed Web of Science ®Google Scholar
• These, A.; Bodi, D.; Ronczka, S.; Lahrssen-Wiederholt, M.; Preiss-Weigert, A. Structural Screening by Multiple Reaction Monitoring as a New Approach for Tandem Mass Spectrometry: Presented for the Determination of Pyrrolizidine Alkaloids in Plants. Anal. Bioanal. Chem. 2013, 405, 9375–9383. DOI: 10.1007/s00216-013-7365-4.
   PubMed Web of Science ®Google Scholar
• Ferreira, S. L. C.; Lemos, V. A.; de Carvalho, V. S.; da Silva, E. G. P.; Queiroz, A. F. S.; Felix, C. S. A.; da Silva, D. L. F.; Dourado, G. B.; Oliveira, R. V. Multivariate Optimization Techniques in Analytical Chemistry—An Overview. Microchem. J. 2018, 140, 176–182. DOI: 10.1016/j.microc.2018.04.002.
   Web of Science ®Google Scholar
• Ferreira, S. L. C.; Bruns, R. E.; Ferreira, H. S.; Matos, G. D.; David, J. M.; Brandão, G. C.; da Silva, E. G. P.; Portugal, L. A.; dos Reis, P. S.; Souza, A. S.; et al. Box-Behnken Design: An Alternative for the Optimization of Analytical Methods. Anal. Chim. Acta 2007, 597, 179–186. DOI: 10.1016/j.aca.2007.07.011.
   PubMed Web of Science ®Google Scholar
• Von Der Ohe, W.; Persano Oddo, L.; Piana, M. L.; Morlot, M.; Martin, P. Harmonized Methods of Melissopalynology. Apidologie 2004, 35, S18–S25. DOI: 10.1051/apido:2004050.
   Google Scholar
• Flade, J.; Beschow, H.; Wensch-Dorendorf, M.; Plescher, A.; Wätjen, W. Occurrence of Nine Pyrrolizidine Alkaloids in Senecio vulgaris L. Depending on Developmental Stage and Season. Plants 2019, 8, 13–54. DOI: 10.3390/plants8030054.
   Web of Science ®Google Scholar
• Boppré, M.; Colegate, S. M.; Edgar, J. A.; Fischer, O. W. Hepatotoxic Pyrrolizidine Alkaloids in Pollen and Drying-Related Implications for Commercial Processing of Bee Pollen. J. Agric. Food Chem. 2008, 56, 5662–5672. DOI: 10.1021/jf800568u.
   PubMed Web of Science ®Google Scholar
• Flores, A. S.; Tozzi, A. M. G. d A.; Trigo, J. R. Pyrrolizidine Alkaloid Profiles in Crotalaria Species from Brazil: Chemotaxonomic Significance. Biochem. Syst. Ecol. 2009, 37, 459–469. DOI: 10.1016/j.bse.2009.06.001.
   Web of Science ®Google Scholar
• Kempf, M.; Beuerle, T.; Bühringer, M.; Denner, M.; Trost, D.; Von Der Ohe, K.; Bhavanam, V. B. R.; Schreier, P. Pyrrolizidine Alkaloids in Honey: Risk Analysis by Gas Chromatography-Mass Spectrometry. Mol. Nutr. Food Res. 2008, 52, 1193–1200. DOI: 10.1002/mnfr.200800051.
   PubMed Web of Science ®Google Scholar
• Kempf, M.; Wittig, M.; Reinhard, A.; von der Ohe, K.; Blacquiere, T.; Raezke, K.-P.; Michel, R.; Schreier, P.; Beuerle, T. Pyrrolizidine Alkaloids in Honey: Comparison of Analytical Methods. Food Addit. Contam. Part A 2011, 28, 332–347. DOI: 10.1080/19440049.2010.521772.
   Web of Science ®Google Scholar
• Lucchetti, M. A.; Glauser, G.; Kilchenmann, V.; Dübecke, A.; Beckh, G.; Praz, C.; Kast, C. Pyrrolizidine Alkaloids from Echium vulgare in Honey Originate Primarily from Floral Nectar. J. Agric. Food Chem. 2016, 64, 5267–5273. DOI: 10.1021/acs.jafc.6b02320.
   PubMed Web of Science ®Google Scholar
• Bodi, D.; Ronczka, S.; Gottschalk, C.; Behr, N.; Skibba, A.; Wagner, M.; Lahrssen-Wiederholt, M.; Preiss-Weigert, A.; These, A. Determination of Pyrrolizidine Alkaloids in Tea, Herbal Drugs and Honey. Food Addit. Contam. Part A 2014, 31, 1886–1895. DOI: 10.1080/19440049.2014.964337.
   PubMed Web of Science ®Google Scholar
• Medicines Agency, E. Public Statement on the Use of Herbal Medicinal Products Containing Toxic, Unsaturated Pyrrolizidine Alkaloids (PAs). Eur. Med. Agency 2014, 44, 1–24.
   Google Scholar
• Moreira, R.; Pereira, D. M.; Valentão, P.; Andrade, P. B. Pyrrolizidine Alkaloids: Chemistry, Pharmacology, Toxicology and Food Safety. Int. J. Mol. Sci. 2018, 19, 1622–1668. DOI: 10.3390/ijms19061668.
   PubMed Web of Science ®Google Scholar
• Schramm, S.; Köhler, N.; Rozhon, W. Pyrrolizidine Alkaloids: Biosynthesis, Biological Activities and Occurrence in Crop Plants. Molecules 2019, 24, 444–498. DOI: 10.3390/molecules24030498.
   PubMed Web of Science ®Google Scholar
• Trigo, J. R.; Leal, I. R.; Matzenbacher, N. I.; Lewinsohn, T. M. Chemotaxonomic Value of Pyrrolizidine Alkaloids in Southern Brazil Senecio (Senecioneae: Asteraceae). Biochem. Syst. Ecol. 2003, 31, 1011–1022. DOI: 10.1016/S0305-1978(03)00038-3.
   Web of Science ®Google Scholar
• Barcelos, S. T. A.; Dall'Oglio, V. M.; de Araújo, A.; Cerski, C. T. S.; Álvares-da-Silva, M. R. Sinusoidal Obstruction Syndrome Secondary the Intake of Senecio brasiliensis: A Case Report. Ann. Hepatol. 2021, 20, 100138. DOI: 10.1016/j.aohep.2019.08.009.
   PubMed Web of Science ®Google Scholar
• Paiva, J. A.; Barata, L. E. S.; Trigo, J. R. Pyrrolizidine Alkaloids in Three Senecio Species from Southern Brazil. Biochem. Syst. Ecol. 2004, 32, 1219–1222. DOI: 10.1016/j.bse.2004.05.004.
   Web of Science ®Google Scholar
• Gardana, C.; Del Bo, C.; Quicazán, M. C.; Corrrea, A. R.; Simonetti, P. Nutrients, Phytochemicals and Botanical Origin of Commercial Bee Pollen from Different Geographical Areas. J. Food Compos. Anal. 2018, 73, 29–38. DOI: 10.1016/j.jfca.2018.07.009.
   Web of Science ®Google Scholar
• Li, Q. Q.; Wang, K.; Marcucci, M. C.; Sawaya, A. C. H. F.; Hu, L.; Xue, X. F.; Wu, L. M.; Hu, F. L. Nutrient-Rich Bee Pollen: A Treasure Trove of Active Natural Metabolites. J. Funct. Foods 2018, 49, 472–484. DOI: 10.1016/j.jff.2018.09.008.
   Web of Science ®Google Scholar
• Kostić, A.; Milinčić, D. D.; Barać, M. B.; Shariati, M. A.; Tešić, ŽL.; Pešić, M. B. The Application of Pollen as a Functional Food and Feed Ingredient—The Present and Perspectives. Biomolecules 2020, 10, 84. DOI: 10.3390/biom10010084.
   PubMed Web of Science ®Google Scholar
• Griffin, C. T.; O’Mahony, J.; Danaher, M.; Furey, A. Liquid Chromatography Tandem Mass Spectrometry Detection of Targeted Pyrrolizidine Alkaloids in Honeys Purchased within Ireland. Food Anal. Methods 2015, 8, 18–31. DOI: 10.1007/s12161-014-9855-1.
   Web of Science ®Google Scholar
• He, Y.; Zhu, L.; Ma, J.; Wong, L.; Zhao, Z.; Ye, Y.; Fu, P. P.; Lin, G. Comprehensive Investigation and Risk Study on Pyrrolizidine Alkaloid Contamination in Chinese Retail Honey. Environ. Pollut. 2020, 267, 115542 DOI: 10.1016/j.envpol.2020.115542.
   PubMed Web of Science ®Google Scholar
• Kast, C.; Dübecke, A.; Kilchenmann, V.; Bieri, K.; Böhlen, M.; Zoller, O.; Beckh, G.; Lüllmann, C. Analysis of Swiss Honeys for Pyrrolizidine Alkaloids. J. Apic. Res. 2014, 53, 75–83. DOI: 10.3896/IBRA.1.53.1.07.
   Web of Science ®Google Scholar
• Ghosh, S.; Jeon, H.; Jung, C. Foraging Behaviour and Preference of Pollen Sources by Honey Bee (Apis mellifera) Relative to Protein Contents. J. Ecol. Environ. 2020, 44, 1–7. DOI: 10.1186/s41610-020-0149-9..
   Google Scholar
• Wiedenfeld, H.; Edgar, J. Toxicity of Pyrrolizidine Alkaloids to Humans and Ruminants. Phytochem. Rev. 2011, 10, 137–151. DOI: 10.1007/s11101-010-9174-0.
   Web of Science ®Google Scholar
• Ma, C.; Liu, Y.; Zhu, L.; Ji, H.; Song, X.; Guo, H.; Yi, T. Determination and Regulation of Hepatotoxic Pyrrolizidine Alkaloids in Food: A Critical Review of Recent Research. Food Chem. Toxicol. 2018, 119, 50–60. DOI: 10.1016/j.fct.2018.05.037.
   PubMed Web of Science ®Google Scholar
• Dübecke, A.; Beckh, G.; Lüllmann, C. Pyrrolizidine Alkaloids in Honey and Bee Pollen. Food Addit. Contam. Part A 2011, 28, 348–358. DOI: 10.1080/19440049.2010.541594.
   Web of Science ®Google Scholar
• European Commission (EU). Comission Regulation (EU) 2020/2040 of 11 December 2020 amending Regulation (EC) 1881/2006 as regards maximum levels of pyrrolizidine alkaloids in certain foodstuffs. European Commission, 2020; pp 1–3. https://eur-lex.europa.eu/legal-content/EN/TXT/HTML/?uri=CELEX:32020R2040&rid=1
   Google Scholar