Ptaquiloside biotoxin in ferns of the genus Pteridium

Authors

  • Massiel Rodríguez-Salazar Instituto Costarricense de Investigacion y Enseñanza en Nutricion y Salud, Cartago, Costa Rica. https://orcid.org/0000-0002-6506-2005
  • Alejandro Chacón-Villalobos Universidad de Costa Rica, Cartago, Costa Rica

DOI:

https://doi.org/10.15517/am.v34i1.49755

Keywords:

weeds, toxicology, cancer, food safety, poisoning

Abstract

Introduction. The ferns of the genus Pteridium are characterized by their wide habitat and adaptive power that allows their establishment in various types of soils and altitudes. They have the ability to produce a toxin called ptaquiloside. Objective. To gather a current body of updated knowledge on the ptaquiloside toxin present in ferns of the genus PteridiumDevelopment. The ferns of the genus Pteridium produce ptaquiloside biotoxin, especially in young phenological stages and in the fronds. The hydrolysis of this toxin at the biological level generates compounds with cytotoxic and genotoxic properties. Ptaquiloside can produce enzootic bovine hematuria, be deposited in the milk of the animal that consumes it and affects the health of dairy consumers. The biotoxin has an immunosuppressive effect in cattle, which can favor the papilloma virus, and also causes blindness in sheep. It is associated with esophageal and gastric cancer in humans living in areas populated by ferns of the genus Pteridium. The carcinogenic effect of ptaquiloside is generated because it causes DNA alkylation at N3 adenine or N7 guanine, 24 h after ingestion. For the eradication of ferns in pastures, mechanical control, biological control, and chemical control, are the most important. Conclusion. The biotoxin ptaquiloside represents a risk to human and animal health, which can spread to soil, water bodies, and food. More research is needed to take measures to reduce its effects.

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References

Adie, H., Richert, S., Kirkman, K., & Lawes, M. (2011). The heat is on: frequent high intensity fire in bracken (Pteridium aquilinum) drives mortality of the sprouting tree Protea caffra in temperate grasslands. Plant Ecology, 212, 2013–2022. http://doi.org/10.1007/s11258-011-9945-8

Aira, M., Tato, A., & Domínguez, J. (2021). Seasonal dynamics of soil nutrients and microbial activity due to colonization by bracken ferns (Pteridium aquilinum (L.) Kuhn) in a pine forest. European Journal of Soil Biology, 103, Article 103295. https://doi.org/10.1016/j.ejsobi.2021.103295

Akomolafe, G. F., & Rahmad, Z. B. (2018). A review on global ferns invasions: mechanisms, management and control. Journal of Research in Forestry, Wildlife and Environment, 10(3), 42–54. https://www.ajol.info/index.php/jrfwe/article/view/178581

Alonso-Amelot, M. E., & Avendaño, M. (2001). Possible association between gastric cancer and bracken fern in Venezuela: an epidemiologic study. International Journal of Cancer, 91(2), 252–259.

Bonadies, F., Borzacchiello, G., Dezzi, S., Nicoletti, R., & Roperto, S. (2004). Mass spectrometric analysis of ptaquiloside, the toxic sesquiterpene from bracken fern. Rapid Communications in Mass Spectrometry, 18(7), 825–828. https://doi.org/10.1002/rcm.1410

Bonadies, F., Berardi, G., Nicoletti, R., Romolo, F. S., De Giovanni, F., Marabelli, R., Santoro, A., Raso, C., Tagarelli, A., Roperto, F., Russo, V., & Roperto, S. (2011). A new, very sensitive method of assessment of ptaquiloside, the major bracken carcinogen in the milk of farm animals. Food Chemistry, 124(2), 660–665. https://doi.org/10.1016/j.foodchem.2010.05.059

Borges, J. A., Camacaro, O., Domínguez, L., & Graterol, A. (2013). Composición bromatológica de Pteridium aquilinum subs. Arachnoideum colectado en el municipio Bolívar, estado de Yaracuy, Venezuela. Revista de la Facultad de Agronomía LUZ, 30, 431–440. https://www.revfacagronluz.org.ve/PDF/julio_septiembre2013/v30n3a2013431440.pdf

Borges, J. A., Dominguez, L., Camacaro, O., & Graterol, A. (2017). Control químico de Pteridium esculentum (G. Forst.) Cockayne (Thomson, 2012) en el Municipio Bolívar, Estado Yaracuy, Venezuela. Bioagro, 29(2), 145–150.

Bulnes, C., & Calderón Tobar, A. (2014). Lesiones asociadas a la Hematuria Enzoótica Bovina (HEB) en animales de matadero (camal) de la Provincia Bolívar, Ecuador. Revista Salud Animal, 36(2), 97–105. http://revistas.censa.edu.cu/index.php/RSA/article/view/442

Calderón, A., Marrero, E., Bulnes, C, & Silva, J. (2015). Diagnóstico epidemiológico y clínico de la hematuria enzoótica bovina en la provincia Bolívar, Ecuador. Talentos, 2(1), 1–12. https://talentos.ueb.edu.ec/index.php/talentos/article/view/75

Calderón Tobar, A., Jiménez Sánchez, A., Sánchez Perera, L. M., Mancebo Dorvigny, B., & Marrero Faz, E. (2014). Risk by human health for invasion of Pteridium arachnoideum, in Bolívar, Ecuador. Ptaquiloside’s content in fronds and in milk. International Journal of Applied Science and Technology, 4(6), 84–94. http://www.ijastnet.com/journal/index/688

Calderón Tobar, A., Marrero Faz, E., Murillo, V., & Vega, V. (2011). Reporte de casos de hematuria enzoótica bovina por ingestión de Pteridium arachnoideum en la región ganadera de San Miguel De Bolívar, provincia Bolívar, Ecuador. Revista Salud Animal, 33(3), 197–202.

Calderón Tobar, A., Sánchez, L. M., Mancebo, B., Marrero, E., Chiriboga, X., & Silva, J. (2014). Residualidad del ptaquilósido en la leche procedente de granjas bovinas en tres cantones de la provincia Bolívar, Ecuador. Revista de Salud Animal, 36(1), 19–27. http://revistas.censa.edu.cu/index.php/RSA/article/view/367

Cepeda, C., & Amoroso, A. (2016). Experiencias de desarrollo sustentable y conservación en la Península de Yucatán (1a ed.). The Nature Conservancy. http://www.biosakbe.com/desarrollo_rural_sustentable/docs/espanol/experiencias.pdf

Corporación Autónoma Regional de Cundinamarca. (2020). Plan de prevención, manejo y control del helecho marranero (Pteridium aquilinum (L.) kuhn) para la jurisdicción de la Corporación Autónoma Regional de Cundinamarca CAR. Corporación Autónoma Regional de Cundinamarca.

Cortinovis, C., & Caloni, F. (2013). Epidemiology of intoxication of domestic animals by plants in Europe. The Veterinary Journal, 197(2), 163–168. https://doi.org/10.1016/j.tvjl.2013.03.007

da Silva Freitas Ribeiro, D., Moura Keller, K., Martins Melos, M., & Soto-Blanco B. (2019). Determination of ptaquiloside in cow’s milk by HPLC-UV. Ciencias Agrarias, 40(4), 1715–1722. https://doi.org/10.5433/1679-0359.2019v40n4p1715

da Silva Freitas Ribeiro, D., Moura Keller, K., & Soto-Blanco, B. (2020). Ptaquiloside and pterosin B levels in mature green fronds and sprouts of Pteridium arachnoideum. Toxins, 12(5), Article 288. https://doi.org/10.3390/toxins12050288

DeLuca, T., Zewdie S. A., Zackrisson, O., Healey, J. R., & Jones, D. L. (2013). Bracken fern (Pteridium aquilinum L. kuhn) promotes an open nitrogen cycle in heathland soils. Plant Soil, 367, 521–534. http://www.jstor.org/stable/42952911

Der, J. P., Thomson, J. A., Stratford, J. K., & Wolf, P. G. (2009). Global chloroplast phylogeny and biogeography of bracken (Pteridium; Dennstaedtiaceae). American Journal of Botany, 96(5), 1041–1049. https://doi.org/10.3732/ajb.0800333

dos Reis Aranha, P. C., Holm Rasmussen, L., Wolf-Jäckel, G. A., Elvang Jensen, H. M. E., Bruun Hansen, H. C. & Friis, C. (2019). Fate of ptaquiloside—A bracken fern toxin—In cattle. PloS ONE Journal, 14(6), Article e0218628. https://doi.org/10.1371/journal.pone.0218628

Duke, S. O. (2015). Proving allelopathy in crop–weed interactions. Weed Science, 63(SP1), 121–132. https://doi.org/10.1614/WS-D-13-00130.1

Eslava-Silva, F. D. J., Jiménez-Durán, K., Jiménez Estrada, M., & Muñiz Díaz de León, M. E. (2020). Morfo-anatomía del ciclo de vida del helecho Pteridium aquilinum (Dennstaedtiaceae) en cultivo in vitro. Revista de Biología Tropical, 68(1), 12–22. http://doi.org/10.15517/rbt.v68i1.36881

Fischer, W. J., Schilter, B., Tritscher, A. M., & Stadler, R. H. (2011). Contaminants of milk and dairy products | environmental contaminants. In J. W. Fuquay (Ed.), Encyclopedia of dairy sciences (2nd ed.; pp. 898–905). Academic Press. https://doi.org/10.1016/B978-0-12-374407-4.00105-9

Fletcher, M. T., Reichmann, K. G., Brock, I. J., McKenzie, R. A., & Blaney, B. J. (2011). Residue potential of norsesquiterpene glycosides in tissues of cattle fed Austral bracken (Pteridium esculentum). Journal of Agricultural and Food Chemistry, 59(15), 8518–8523. https://doi.org/10.1021/jf201342t

García-Jorgensen, D. B., Hansen, H. C. B., Abrahamsen, P., & Diamantopoulos, E. (2020). A novel model concept for modelling the leaching of natural toxins: results for the case of ptaquiloside. Environmental Science: Processes & Impacts, 22(8), 1768–1779. https://doi.org/10.1039/D0EM00182A

García-Jorgensen, D. B., Diamantopoulos, E., Kisielius, V., Rosenfjeld, M., Holm Rasmussen, L., Strobel, B. W., & Hansen, H. C. B. (2021). Bracken growth, toxin production and transfer from plant to soil: a 2-year monitoring study. Environmental Sciences Europe, 33, Article 45. https://doi.org/10.1186/s12302-021-00484-0

Ghorbani, J., Das, P. M., Das, A. B., Hughes, J. M., McAllister, H. A., Pallai, S. K., Pakeman, R. J., Marre, R. H., & Le Duc, M. G. (2003). Effects of restoration treatments on the diaspore bank under dense Pteridium stands in the UK. Applied Vegetation Science, 6(2), 189–198. https://doi.org/10.1111/j.1654-109X.2003.tb00579.x

Ghorbani, J., Le Duc, M. G., McAllister, H. A., Pakeman, R. J., & Marrs, R. H. (2007). Effects of experimental restoration on the diaspore bank of an upland moor degraded by Pteridium aqualinum invasion. Land Degradation & Development, 18(6), 659–669. https://doi.org/10.1002/ldr.804

Gil da Costa, R. M., Bastos, M. M. S. M., Oliveira, P. A., & Lopes, C. (2012). Bracken- associated human and animal health hazards: Chemical, biological and pathological evidence. Journal of Hazardous Materials, 203-204, 1–12. https://doi.org/10.1016/j.jhazmat.2011.12.046

Gil da Costa, R. M., Coehlo, P., Sousa, R., Bastos, M. M. S. M., Porto, B., Teixeira, J. P., Malheiro, I., & Lopes, C. (2012). Multiple genotoxic activities of ptaquiloside in human lymphocytes: aneugenesis, clastogenesis and induction of sister chromatid exchange. Mutatio Research, 30(1), 77–81. https://doi.org/10.1016/j.mrgentox.2012.04.010

Gil da Costa, R. M., Neto, T., Estêvão, D., Moutinho, M., Félix, A., Medeiros, R., Lopes, C., Bastos M. M. S. M., & Oliveira, P. A. (2020). Ptaquiloside from bracken (Pteridium spp.) promotes oral carcinogenesis initiated by HPV16 in transgenic mice. Food & Function, 11(4), 3298–3305. https://doi.org/10.1039/D0FO00207K

Gomes, J., Magalhães, A., Michel, V., Amado, I. F., Aranha, P., Ovesen, R. G., Hansen, H. C. B., Gärtner, F., Reis, A. & Touati, E. (2012). Pteridium aquilinum and its ptaquiloside toxin induce DNA damage response in gastric epithelial cells, a link with gastric carcinogenesis. Toxicological Sciences, 126(1), 60–71. https://doi.org/10.1093/toxsci/kfr329

Hama, J. R., & Strobel, B. W. (2019). Pyrrolizidine alkaloids quantified in soil and water using UPLC-MS/MS. RSC Advances, 52(9), 30350–30357. https://doi.org/10.1039/C9RA05301H

Holm Rasmussen, L (2021). Presence of the carcinogen ptaquiloside on fern-based food products and traditional medicine: four cases of human exposure. Current Research in Food Science, 4, 557–564. https://doi.org/10.1016/j.crfs.2021.08.004

Holm Rasmussen, L., Bruun Hansen, H. C., & Lauren, D. (2005). Sorption, degradation and mobility of ptaquiloside, a carcinogenic Bracken (Pteridium sp.) constituent, in the soil environment. Chemosphere, 58(6), 823–835. https://doi.org/10.1016/j.chemosphere.2004.08.088

Holm Rasmussen, L., Schmidt, B., & Sheffield, E. (2013). Ptaquiloside in bracken spores from Britain. Chemosphere, 90(10), 2539–2541. https://doi.org/10.1016/j.chemosphere.2012.10.092

Hsueh, M. -T, Fan, C., & Chang, W. -L. (2020). Allelopathic Effects of Bidens pilosa L. var. radiata Sch. Bip. on the tuber sprouting and seedling growth of Cyperus rotundus L. Plants, 9(6), Article 742. https://doi.org/10.3390/plants9060742

Issaoui, H., Charrier, F., & Bouhtoury, E. (2020). Bio-based products from wood materials. In C. M. Galanakis (Ed.), Biobased products and industries (Chapter 7, pp. 245–277). Elsevier Inc. https://doi.org/10.1016/B978-0-12-818493-6.00007-5

Jatoba, L. D. J., Varela, R. M., Gonzalez Molinillo, J. M., Ud Din, Z., Juliano Gualteri, S. C., Rodrigues-Filho, E., & Macías, F. A. (2016). Allelopathy of bracken fern (Pteridium arachnoideum): new evidence from green fronds, litter, and soil. PlosOne, 11(8), Article e0161670. https://doi.org/10.1371/journal.pone.0161670

Latorre, A. O., Caniceiro, B. D., Fukumasu, H., Gardner, D. R., Lopes, F. M., Wysochi Jr., H. L., da Silva, T., Haraguchi, M., Bressan, F. F., & Górniak, S. L. (2013). Ptaquiloside reduces NK cell activities by enhancing metallothionein expression, which is prevented by selenium. Toxicology, 304, 100–108. http://doi.org/10.1016/j.tox.2012.12.010

Leitolis, A., Gimenez de Souza, F., Freitas, K., Barddal, H., Rauh, L., Franco, J., & Pereira, L. F. (2017). Tissue damage and embryonic malformation induced by aqueous extract of Pteridium aquilinum on chorioallantoic membrane of chick embryo (CAM). Ciencias Agrarias, 38(3), 1451–1460. https://doi.org/10.5433/1679-0359.2017v38n3p1451

Lévy, M. (2020). Polioencephalomalacia in ruminants (Cerebrocortical Necrisis). MSD Veterinary manual. https://msdmnls.co/3Cu0oPL

Lu, J., Peng, C., Cheng, C., Liu, P., Ma, Q., & Shu, J. (2019). Four new Pterosins from Pteris cretica and their cytotoxic activities. Molecules, 24(15), Article 2767. https://doi.org/10.3390/molecules24152767

Marchiosi, R., Wanderley D. D. S., Polimeni Constantin, R. Barbosa de Lima, R., Soares, A. R., Finger-Teixeira, A., Rodrigues Mota, T., de Oliviera, M., Foletto-Felipe, M. D. P., Abrahao, J, & Ferrarese-Filho, O. (2020). Biosynthesis and metabolicactions of simple phenolic acids in plants. Phytochemistry Reviews, 19, 865–906. https://doi.org/10.1007/s11101-020-09689-2

Maren, I. E., Vandvik, V., & Ekelund, K. (2008). Effectiveness of chemical and mechanical bracken Pteridium aquilinum control treatments in northern coastal heathlands on the island of Lygra, Hordaland, Norway. Conservation Evidence, 5, 12–17.

Marín, R. E. (2011). Aportes al conocimiento de las plantas tóxicas para el ganado de la provincia de Jujuy. Ministerio de Producción de Jujuy, & Dirección Provincial de Desarrollo Ganadero.

Marín, R. E. (2019). Intoxicación por Pteridium aquilinum en bovinos en Jujuy, Argentina: Caracterización clínica y patológica. Editorial Académica Española.

Marrero Faz, E., & Calderón Tobar, A. (2012). Plantas tóxicas e inocuidad alimentaria: Hematuria Enzoótica Bovina por Pteridium spp. un problema relevante de salud. Revista de Salud Animal, 34(3), 137–143. http://revistas.censa.edu.cu/index.php/RSA/article/view/3

Marrs, R. H., & Watt, A. S. (2006). Biological flora of the British Isles: Pteridium aquilinum (L.) Kuhn. Journal of Ecology, 94(6), 1272–1321. https://doi.org/10.1111/j.1365-2745.2006.01177.x

Medeiros-Fonseca, B., Abreu-Silva, A. L., Medeiros, R., Oliviera, P. A., & Gil da Costa, R. M. (2021). Pteridium spp. and bovine papillomavirus: partners in cancer. Frontiers in Veterinary Science, 8, Article 758720. https://doi.org/10.3389/fvets.2021.758720

Mejía Pacheco, L. M., & Malo Cevallos, I. P. (2020). Diagnóstico de la incidencia de Hematuria Enzoótica Bovina de bovinos en producción de tres zonas ganaderas. Revista Metropolitana de Ciencias Aplicadas, 3(1), 76–86. https://remca.umet.edu.ec/index.php/REMCA/article/view/234/276

Miatto, R. C., Silva, I. A., Silva-Matos, D. M., & Marrs, R.H. (2011). Woody vegetation structure of Brazilian Cerrado invaded by Pteridium arachnoideum (Kaulf.) Maxon (Dennstaedtiaceae). Flora, 206(8), 757–762. https://doi.org/10.1016/j.flora.2010.12.001

Miesner, M. D. (2009). Bovine enzootic hematuria. In D. E. Anderson, & D. Rings (Eds.), Current veterinary therapy: Food animal practice (Chapter 71, 5th ed., pp. 330). Saunders Elsevier. https://doi.org/10.1016/B978-1-4160-3591-6.X0135-2

Ministerio de Salud. (2019). Análisis de la situación de salud 2018. https://bit.ly/3wEasUr

Mira, Y. D., Ramírez, L. A., Londoño, L. F., & Castañeda, D. A. (2021). Allelopathic effects of common bracken (Pteridium aquilinum (L.) Kuhn) on germination and growth of economically important weeds. Chilean Journal of Agricultural & Animal Science, 37(3), 290–300. https://doi.org/10.29393/CHJAAS37-30AEYD40030

Mohammad, R. H., Nur-E-Alam, M., Lahmann, M., Parveen, I., Tizzard, G. J., Coles, S. J., Fowler, M., Drake, A. F., Heyes, D., & Thoss, V. (2016). Isolation and characterisation of 13 pterosins and pterosides from bracken (Pteridium aquilinum (L.) Kuhn) rhizome. Phytochemistry, 128, 82–94. https://doi.org/10.1016/j.phytochem.2016.05.001

Oliveira Latorre, A., Furlan, M. S., Sakai, M., Fukumasu, H., Machado Hueza, I., Haraguchi, M., & Lima Górniak, S. (2009). Immunomodulatory effects of Pteridium aquilinum on natural killer cell activity and select aspects of the cellular immune response of mice. Journal of Immunotoxicology, 6(2), 104–114. https://doi.org/10.1080/15476910902972465

Panter, K. E., Gardner, D. R., Lee, S. T., Pfister, J. A., Ralphs, M. H., Stegelmeier, B. L., & James, L. F. (2007). Important poisonous plants of the United States. In R. C. Gupta (Ed.), Veterinary toxicology: Basic and clinical principles (Chapter 66, 3rd ed., pp. 837–889). Academic Press. https://doi.org/10.1016/B978-0-12-811410-0.00061-1

Perrie, L. R., Shepherd, L. D., & Brownsey, P. J. (2015). An expanded phylogeny of the Dennstaedtiaceae ferns: Oenotrichia falls within a non-monophyletic Dennstaedtia, and Saccoloma is polyphyletic. Australian Systematic Botany, 28(4), 256–264. https://doi.org/10.1071/SB15035

Petitjean, A., Mathe, E., Kato, S., Ishioka, C., Tavtigian, S. V., Hainaut, P., & Olivier, M. (2007). Impact of mutant p53 functional properties on TP53 mutation patterns and tumor phenotype: lessons from recent developments in the IARC TP53 database. Human Mutation, 28(6), 622–629. https://doi.org/10.1002/humu.20495

Plessers, E., Pardon, B., Deprez, P., De Backer, P., & Croubels, S. (2013). Acute hemorrhagic syndrome by bracken poisoning in cattle in Belgium. Tijdschrift, 82(1), 31–37. https://doi.org/10.21825/vdt.v82i1.16725

Ramwell, C. T., van Beinum, W., Rowbotham, A., Parry, H., Fera, C.R., Parson, S.A., Luo, W., & Evans, G. (2010). Ptaquiloside & other bracken toxins: a preliminary risk assessment (Final Report). The Food and Environment Research Agency. https://cdn.dwi.gov.uk/wp-content/uploads/2020/10/27111037/DWI70-2-237.pdf

Rasmussen, L. H., Donnelly, E., Strobel, B. W., Holm, P. E., & Hansen, H. C. B. (2015). Land management of bracken needs to account for bracken carcinogens - a case study from Britain. Journal of Environmental Management, 151, 258–266. https://doi.org/10.1016/j.jenvman.2014.12.052

Rasmussen, L. H., Kroghsbo, S., Frisvad, J. C., & Hansen, H. C. B. (2003). Occurrence of the carcinogenic bracken constituent ptaquiloside in fronds, topsoils and organic soil layers in Denmark. Chemosphere, 51(2), 117–127. https://doi.org/10.1016/S0045-6535(02)00694-X

Reis Aranha, P. C., Bruun Hansen, H. C., Holm Rasmussen, L., Strobel, B., & Friis, C. (2014). Determination of ptaquiloside and pterosin B derived from bracken (Pteridium aquilinum) in cattle plasma, urine and milk. Journal of Chromatography B: Analytical Technologies in the Biomedical and Life Sciences, 951–952, 44–51. https://doi.org/10.1016/j.jchromb.2014.01.022

Riet-Correa, F., Medeiros, R., Pfister, J., Schild, A. L., & Dantas, A. (2009). Poisonings by plants, mycotoxins and related substances in Brazilian livestock. Editora da Universidade Federal de Campina Grande.

Rincón, D. F., Díaz, G. J., & Gardner, D. R. (2016). Detection of Ptaquilosides in different 23honologic stages of Bracken fern (Pteridium aquilinum) and analysis of mik samples in farms with hematuria in Tolima, Colombia. Revista CES Medicina Veterinaria y Zootecnia, 11(1), 72–77. https://revistas.ces.edu.co/index.php/mvz/article/view/3820

Ríos-Gutiérrez, M., Domingo, L. R., & Alonso-Amelot, E. (2017). A DFT study of the conversion of ptaquiloside, a bracken fern carcinogen, to Pterosin B in neutral and acidic aqueous medium. Chemistry Select, 2(26), 8178–8186. https://doi.org/10.1002/slct.201701409

Rocha, J. F., Santos, B. B. N., Galvão, A., Marques, T. O., Silva, L. R. L., França, T. N., & Peixoto, P. V. (2022). Occurrence of enzootic hematuria in buffaloes in Brazil: epidemiological, clinical, and pathological aspects. Pesquisa Veterinárina Brasileira, 42, Article e06875. https://doi.org/10.1590/1678-5150-PVB-6875

Rodriguez, A. M., Derita, M. G., Borkosky, S. A., Socolsky, C., Bardón, A., & Hernández, M. A. (2018). Bioactive farina of Notholaena sulphurea (Pteridaceae): Morphology and histochemistry of glandular trichomes. Flora, 240, 144–151. https://doi.org/10.1016/j.flora.2018.01.008

Sánchez, A., Villarroel, R., Pino, D., García, D., Molero, G., & Carrasco de D, D. (2003). Evaluación comparativa de diferentes métodos de control de la hematuria enzoótica bovina. Revista Científica FCV-LUZ, 13(1), 33–37. https://produccioncientificaluz.org/index.php/cientifica/article/view/14958/14935

Santos, C., Vilanova, M., Medeiros, R., & Gil da Costa, R. M. (2017). HPV-transgenic mouse models: Tools for studying the cancer-associated immune response. Virus Research, 2, 235–249. https://doi.org/10.1016/j.virusres.2017.04.001

Scala, C., Ortiz, K., Catinaud, J., & Lemberger, K. (2014). Hematuria and urinary bladder lesions compatible with bracken fern (Pteridium aquilinum) intoxication in captive fallow deer (Dama dama). Journal of Zoo and Wildlife Medicine, 45(2), 380–385. https://doi.org/10.1638/2013-0274R1.1

Schwartsburd, P. B. (2017). Flora of Espíritu Santo: Dennstaedtiaceae. Rodriguésia, 68(5), 1559–1575. https://doi.org/10.1590/2175-7860201768504

Schubbert, S., Shannon, K., & Bollag, G. (2007). Hyperactive Ras in developmental disorders and cancer. Nature Reviews Cancer, 7, 295–308. https://doi.org/10.1038/nrc2109

Scottish Environmental and Rural Services. (2008). Bracken control: a guide to best practice. SEARS natural Scotland. https://bit.ly/3ajMQf9

Senyanzobe, J. M. V., Mulei, J. M., Bizuru, E., & Nsengimuremyi, C. (2020). Impact of Pteridium aquilinum on vegetation in Nyungwe Forest, Rwanda. Heliyon, 6(9), Article e04806. https://doi.org/10.1016%2Fj.heliyon.2020.e04806

Seva, J. I., Mas, A., Sanes, J. M., Trigueros, I., & Pallarés, F. J. (2010). Poliencefalomalacia asociada a acidosis metabólica en bovino de lidia. Anales de Veterinaria de Murcia, 26, 91–96. https://revistas.um.es/analesvet/article/view/125081

Skourti-Stathaki, E., Clauson-Kaas, F., Brandt, K. K., Holm Rasmussen, L., & Bruun Hansen, H. C. (2016). Dissipation of pterosin B in acid soils – tracking the fate of the bracken fern carcinogen ptaquiloside. Chemosphere, 165, 453–459. https://doi.org/10.1016/j.chemosphere.2016.09.050

Skrbic, N., Pedersen, A. -K., Christensen, S. C. B., Bruun Hansen, H. C., & Holm Rasmussen, L. (2020). A novel method for determination of the natural toxin ptaquiloside in ground and drinking water. Water, 12(10), Article 2852. http://doi.org/10.3390/w12102852

Smith, J., Mun Tho, L., Xu, N., & Gillespie, D. A. (2010). The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Advances in Cancer Research, 108, 73–112. https://doi.org/10.1016/B978-0-12-380888-2.00003-0

Ssali, F., Moe, S. R., & Sheil, D. (2019). The differential effects of bracken (Pteridium aquilinum (L.) Kuhn) on germination and seedling performance of tree species in the African tropics. Plant Ecology Journal, 220, 41–55. https://doi.org/10.1007/s11258-018-0901-8

Suazo-Ortuño, I., Lopez-Toledo, L., Alvarado-Díaz, J., & Martínez-Ramos, M. (2015). Land-use change dynamics, soil type and species forming mono-dominant patches: The case of Pteridium aquilinum in a neotropical rain forest region. Biotropica, 47(1), 18–26. https://doi.org/10.1111/btp.12181

Tampa Sompila, A. W. G., Moussounga, J. E., Madiélé-Mabika, A. B., Pambou-Tobi, N. P. G., Diakabana, P., Miakayizila, B. D. E., Dzondo-Gadet, M., & Silou, T. (2019). Conservation and analysis of the physicochemical parameters of a Congo food plant alicamentary [Pteridium aquilinum (L.) Kuhn]. International Journal of Current Microbiology and Applied Sciences, 8(9), 247–256. https://doi.org/10.20546/ijcmas.2019.809.030

Tourchi Roudsari, M., Reza Bahrami, A., Dehghani, A., Iranshahi, M., Moghadam Matin, M., & Mohmoudi, M. (2012). Bracken-fern extracts induce cell cycle arrest and apoptosis in certain cancer cell lines. Asian Pacific Journal of Cancer Prevention, 13(12), 6047–6053. https://doi.org/10.7314/apjcp.2012.13.12.6047

Tourchi-Roudsari, M. (2014). Multiple effects of bracken fern under in vivo and in vitro conditions. Asian Pacific Journal of Cancer Prevention, 15(18), 7507–7509. http://doi.org/10.7314/APJCP.2014.15.18.7505

Ugochukwu, I. C. I. (2019). Bracken fern toxicity and its associated clinicopathological effects in humans and animals: a review. Comparative Clinical Pathology, 28, 593–597. https://doi.org/10.1007/s00580-018-2636-2

Valdez-Ramírez, C., Levy-Tacher, S. I., León-Martínez, N. S., Navarrete-Gutiérrez, D. A., & Ortiz-Ceballos, A. I. (2020). Cambios químicos y biológicos del suelo provocados por Pteridium aquilinum (L.) Kuhn en áreas de influencia de la reserva de la biosfera de Calakmul, Campeche. Terra Latinoamericana, 38, 289–300. https://doi.org/10.28940/terra.v38i2.464

Van Driesche, R. G., Hoddle, M. S., & Center, T. D. (2007). Control de plagas y malezas por enemigos naturales. USDA Forest Service.

Vargas Peixoto, P., do Nascimento França, T., Barros, C. S. L., & Hubinger Tokarnia, C. (2003). Histopathological aspects of bovine enzootic hematuria in Brazil. Pesquisa Veterinaria Brasileira, 23(2), 65–81. https://doi.org/10.1590/S0100-736X2003000200004

Verde, G., García, M., Chavera, A., Gonzáles, C., & Falcón, N. (2017). Diagnóstico clínico de la hematuria vesical enzoótica bovina por uroanálisis de la provincia de Oxapampa, Perú. Revista de Investigaciones Veterinarias del Perú, 28(3), 522–529. http://doi.org/10.15381/rivep.v28i3.13286

Vetter, J. A. (2009). A biological hazard of our age: bracken fern [Pteridium aquilinum (L.) Kuhn] - a review. Acta Veterinaria Hungarica, 57(1), 183–196. https://doi.org/10.1556/avet.57.2009.1.18

Virgilio, A., Sinisi, A., Russo, V., Gerardo, S., Santoro, A., Galeone, A., Taglialatela-Scafati, O., & Roperto, F. (2015). Ptaquiloside, the major carcinogen of bracken fern, in the pooled raw milk of healthy sheep and goats: an underestimated, global concern of food safety. Journal of Agricultural and Food Chemistry, 63(19), 4886–4892. https://doi.org/10.1021/acs.jafc.5b01937

Waret-Szkuta, A., Jégou, L., Lucas, M. N., Gaide, N., Morvan, H., & Martineau, G. -P. (2021). A case of eagle fern (Pteridium aquilinum) poisoning on a pig farm. Porcine Health Management, 7, Article 2. https://doi.org/10.1186/s40813-020-00185-9

Wolf, P., Rowe, C., Kinosian, S., Der, J., Lockhart, P., Shepherd, L., McLenachan, P., & Thomson, J. (2019). Worldwide relationships in the fern genus Pteridium (bracken) based on nuclear genome markers. American Journal of Botany, 106(10), 1365–1376. https://doi.org/10.1002%2Fajb2.1365

Wu, J. S., Clauson-Kaas, F., Lindqvist, D. N., Holm-Rasmussen, L., Strobel, B., & Bruun-Hansen, H. C. (2021). Does the natural carcinogen ptaquiloside degrade readily in groundwater? Environmental Sciences Europe, 33, Article 24. https://doi.org/10.1186/s12302-021-00468-0

Yamada, K., Ojika, M., & Kigoshi, H. (2007). Ptaquiloside, the major toxin of bracken, and related terpene glycosides: chemistry, biology and ecology. Natural Product Reports, 24(4), 798–813. https://doi.org/10.1039/b614160a

Yurdakok, B., Kismali, G., & Ozen, D. (2014). Ptaquiloside-induced citotoxicity in Crandall feline fidney and HGC-27 cells. Oncology Letters, 8(4), 1839–1843. https://doi.org/10.3892/ol.2014.2378

Zaccone, C., Cavoski, I., Costi, R., Sarais, G., Caboni, P., Traversa, A., & Miano, T. (2014). Ptaquiloside in Pteridium aquilinum subsp. aquilinum and corresponding soils from the South of Italy: Influence of physical and chemical features of soils on its occurrence. Science of The Total Environment, 496, 365–372. https://doi.org/10.1016/j.scitotenv.2014.07.046

Published

2022-10-21

How to Cite

Rodríguez-Salazar, M., & Chacón-Villalobos, A. (2022). Ptaquiloside biotoxin in ferns of the genus Pteridium. Agronomía Mesoamericana, 34(1), 49755. https://doi.org/10.15517/am.v34i1.49755

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