TOCOSH FLOUR (Solanum tuberosum L.): A Toxicological Assessment of Traditional Peruvian Fermented Potatoes
Abstract
:1. Introduction
2. Material and Methods
2.1. Collection of Plant Material
2.2. Preparation of the Tocosh Flour
2.3. Phytochemical Analysis
2.4. Experimental Animals
2.5. Sub-Acute Toxicity at Repeated Dose for 28 Days
2.6. Acute Oral Toxicity—Fixed-Dose Study Procedure
2.7. Histopathological Analysis
2.8. Prediction of Drug-Likeness Properties for Steroidal Glycoalkaloids: α-Solanin, α-Chaconine and Solanidine
- Permeability lower than 25: low permeability.
- Permeability between 25 and 500: medium permeability.
- Permeability higher 500: high permeability.
2.9. Statistical Analysis
3. Results
3.1. Phytochemical Analysis
3.2. Repeated Dose Toxicity Study for 28 Days
3.3. Acute Oral Toxicity—Fixed Dose Procedure Study
3.4. Prediction of Drug-Likeness Properties for Steroidal Glycoalkaloids: α-Solanin, α-Chaconine and Solanidine
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability
Conflicts of Interest
References
- Hardigan, M.A.; Laimbeer, F.P.E.; Newton, L.; Crisovan, E.; Hamilton, J.P.; Vaillancourt, B.; Wiegert-Rininger, K.; Wood, J.C.; Douches, D.S.; Farré, E.M.; et al. Genome diversity of tuber-bearing solanum uncovers complex evolutionary history and targets of domestication in the cultivated potato. Proc. Natl. Acad. Sci. USA 2017. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Berdugo-Cely, J.; Valbuena, R.I.; Sánchez-Betancourt, E.; Barrero, L.S.; Yockteng, R. Genetic diversity and association mapping in the colombian central collection of solanum tuberosum L. Andigenum group using SNPs markers. PLoS ONE 2017. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Velásquez-Milla, D.; Casas, A.; Torres-Guevara, J.; Cruz-Soriano, A. Ecological and socio-cultural factors influencing in situ conservation of crop diversity by traditional andean households in Peru. J. Ethnobiol. Ethnomed. 2011. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mayta-Tovalino, F.; Sedano-Balbin, G.; Romero-Tapia, P.; Alvítez-Temoche, D.; álvarez-Paucar, M.; Gálvez-Calla, L.; Sacsaquispe-Contreras, S. Development of new experimental dentifrice of peruvian solanum tuberosum (Tocosh) fermented by water stress: Antibacterial and cytotoxic activity. J. Contemp. Dent. Pract. 2019. [Google Scholar] [CrossRef]
- Mosso, A.L.; Jimenez, M.E.; Vignolo, G.; LeBlanc, J.G.; Samman, N.C. Increasing the folate content of tuber based foods using potentially probiotic lactic acid bacteria. Food Res. Int. 2018. [Google Scholar] [CrossRef] [PubMed]
- LeBlanc, J.G.; Vignolo, G.; Todorov, S.D.; de Giori, G.S. Indigenous fermented foods and beverages produced in Latin America. In Food Intake: Regulation, Assessing and Controlling; Nova Science Publishers, Inc.: Hauppauge, NY, USA, 2013. [Google Scholar]
- Langkilde, S.; Mandimika, T.; Schrøder, M.; Meyer, O.; Slob, W.; Peijnenburg, A.; Poulsen, M. A 28-day repeat dose toxicity study of steroidal glycoalkaloids, α-solanine and α-chaconine in the Syrian Golden hamster. Food Chem. Toxicol. 2009. [Google Scholar] [CrossRef]
- Barceloux, D.G. Potatoes, Tomatoes, and Solanine Toxicity (Solanum tuberosum L., Solanum lycopersicum L.). Dis. Mon. 2009, 55, 391–402. [Google Scholar] [CrossRef]
- Friedman, M. Potato glycoalkaloids and metabolites: Roles in the plant and in the diet. J. Agric. Food Chem. 2006, 54, 8655–8681. [Google Scholar] [CrossRef]
- Chen, Z.; Miller, A.R. Steroidal alkaloids in solanaceous vegetable crops. Hortic. Rev. 2010, 171–196. [Google Scholar] [CrossRef]
- Herrera-Calderon, O.; Arroyo-Acevedo, J.L.; Rojas-Armas, J.; Chumpitaz-Cerrate, V.; Figueroa-Salvador, L.; Enciso-Roca, E.; Tinco-Jayo, J.A. Phytochemical screening, total phenolic content, antioxidant and cytotoxic activity of chromolaena laevigata on human tumor cell lines. Annu. Res. Rev. Biol. 2017. [Google Scholar] [CrossRef] [Green Version]
- OECD/OECDE. Test No. 407: Repeated Dose 28-Day Oral Toxicity Study in Rodents; OECD Publishing: Paris, France, 2008. [Google Scholar]
- OECD. Test No. 420: Acute oral toxicity-fixed dose procedure. Oecd Guidel. Test. Chem. 2002. [Google Scholar] [CrossRef]
- Enciso-Roca, E.; Aguilar-Felices, E.J.; Tinco-Jayo, J.A.; Arroyo-Acevedo, J.L.; Herrera-Calderon, O.; Aguilar-Carranza, C.; Justil, H.G. Effects of acute and sub-acute oral toxicity studies of ethanol extract of tanacetum parthenium (L) Sch. Bip. Aerial parts in mice and rats. Annu. Res. Rev. Biol. 2017. [Google Scholar] [CrossRef]
- Butina, D.; Segall, M.D.; Frankcombe, K. Predicting ADME properties in silico: Methods and models. Drug Discov. Today 2002. [Google Scholar] [CrossRef]
- Morris, S.C.; Lee, T.H. The toxicity and teratogenicity of Solanaceae glycoalkaloids, particularly those of the potato (Solanum tuberosum): A review. Food Technol. Aust. 1984, 36, 195–202. [Google Scholar]
- Romanucci, V.; Pisanti, A.; Di Fabio, G.; Davinelli, S.; Scapagnini, G.; Guaragna, A.; Zarrelli, A. Toxin levels in different variety of potatoes: Alarming contents of α-chaconine. Phytochem. Lett. 2016. [Google Scholar] [CrossRef]
- Crawford, L.; Myhr, B. A preliminary assessment of the toxic and mutagenic potential of steroidal alkaloids in transgenic mice. Food Chem. Toxicol. 1995. [Google Scholar] [CrossRef]
- Abduh, S.B.M.; Leong, S.Y.; Agyei, D.; Oey, I. Understanding the properties of starch in potatoes (Solanum tuberosum var. Agria) after being treated with pulsed electric field processing. Foods 2009. [Google Scholar] [CrossRef] [Green Version]
- Nielsen, S.D.; Schmidt, J.M.; Kristiansen, G.H.; Dalsgaard, T.K.; Larsen, L.B. Liquid chromatography mass spectrometry quantification of α-solanine, α-chaconine, and solanidine in potato protein isolates. Foods 2020. [Google Scholar] [CrossRef] [Green Version]
- Cui, L.; Tian, Y.; Tian, S.; Wang, Y.; Gao, F. Preparation of potato whole flour and its effects on quality of flour products: A review. Grain Oil Sci. Technol. 2018. [Google Scholar] [CrossRef] [Green Version]
- Patil, B.C.; Sharma, R.P.; Salunkhe, D.K.; Salunkhe, K. Evaluation of solanine toxicity. Food Cosmet. Toxicol. 1972. [Google Scholar] [CrossRef]
- Lau, J.K.C.; Zhang, X.; Yu, J. Animal models of non-alcoholic fatty liver disease: Current perspectives and recent advances. J. Pathol. 2016. [Google Scholar] [CrossRef] [PubMed]
- Brunt, E.M.; Tiniakos, D.G. Histopathology of nonalcoholic fatty liver disease. World J. Gastroenterol. 2010. [Google Scholar] [CrossRef] [PubMed]
- Greaves, P. Histopathology of Preclinical Toxicity Studies: Interpretation and Relevance in Drug Safety Evaluation, 4th ed.; Academic Press: Amsterdam, The Netherlands, 2011. [Google Scholar]
- Hashimoto, N.; Ito, Y.; Han, K.H.; Shimada, K.I.; Sekikawa, M.; Topping, D.L.; Bird, A.R.; Noda, T.; Chiji, H.; Fukushima, M. Potato pulps lowered the serum cholesterol and triglyceride levels in rats. J. Nutr. Sci. Vitaminol. 2006. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, Y.; Chiriboga, D.E.; Olendzki, B.C.; Li, W.; Leung, K.; Hafner, A.R.; Li, Y.; Ockene, I.S.; Hebert, J.R. Association between Carbohydrate Intake and Serum Lipids. J. Am. Coll. Nutr. 2006. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, S.; Panter, K.E.; Gaffield, W.; Evans, R.C.; Bunch, T.D. Effects of steroidal glycoalkaloids from potatoes (Solanum tuberosum) on in vitro bovine embryo development. Anim. Reprod. Sci. 2005. [Google Scholar] [CrossRef] [PubMed]
- Zhou, X.; Gao, Q.; Praticò, G.; Chen, J.; Dragsted, L.O. Biomarkers of tuber intake. Genes Nutr. 2019. [Google Scholar] [CrossRef] [Green Version]
- Friedman, M. Analysis of biologically active compounds in potatoes (Solanum tuberosum), tomatoes (Lycopersicon esculentum), and jimson weed (Datura stramonium) seeds. J. Chromatogr. A 2004. [Google Scholar] [CrossRef]
- Friedman, M.; Rayburn, J.R.; Bantle, J.A. Structural Relationships and Developmental Toxicity of Solanum Alkaloids in the Frog Embryo Teratogenesis Assay-Xenopus. J. Agric. Food Chem. 1992. [Google Scholar] [CrossRef]
- Connors, N.J.; Glover, R.L.; Stefan, C.; Patterson, D.; Wong, E.; Milstein, M.; Swerdlow, M.; Hoffman, R.S.; Nelson, L.S.; Smith, S.W. Biological and botanical confirmation of solanaceous glycoalkaloid poisoning by susumber berries (Solanum torvum). Clin. Toxicol. 2014. [Google Scholar] [CrossRef]
- Nigg, H.N.; Ramos, L.E.; Graham, E.M.; Sterling, J.; Brown, S.; Cornell, J.A. Inhibition of human plasma and serum butyrylcholinesterase (EC 3.1.1.8) by α-chaconine and α-solanine. Fundam. Appl. Toxicol. 1996. [Google Scholar] [CrossRef]
- Gaffield, W.; Keeler, R.F. Induction of terata in hamsters by solanidane alkaloids derived from Solanum tuberosum. Chem. Res. Toxicol. 1996. [Google Scholar] [CrossRef] [PubMed]
- Lin, T.; Oqani, R.K.; Lee, J.E.; Kang, J.W.; Kim, S.Y.; Cho, E.S.; Jeong, Y.D.; Baek, J.J.; Jin, D. Il α-Solanine impairs oocyte maturation and quality by inducing autophagy and apoptosis and changing histone modifications in a pig model. Reprod. Toxicol. 2018. [Google Scholar] [CrossRef] [PubMed]
- Bell, D.P.; Gibson, J.G.; McCarroll, A.M.; McClean, G.A. Embryotoxicity of solanine and aspirin in mice. J. Reprod. Fertil. 1976. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yamashoji, S.; Matsuda, T. Synergistic cytotoxicity induced by α-solanine and α-chaconine. Food Chem. 2013. [Google Scholar] [CrossRef]
- Al Sinani, S.S.S.; Eltayeb, E.A. The steroidal glycoalkaloids solamargine and solasonine in solanum plants. South. Afr. J. Bot. 2017. [Google Scholar] [CrossRef]
- Nair, A.; Jacob, S. A simple practice guide for dose conversion between animals and human. J. Basic Clin. Pharm. 2016. [Google Scholar] [CrossRef] [Green Version]
Organs | Control Group | Tocosh Flour Dose: 1000 mg/kg |
---|---|---|
Male rats | n = 5 | n = 5 |
Brain | 0.70 ± 0.03 | 0.65 ± 0.01 |
Heart | 0.35 ± 0.00 | 0.37 ± 0.05 |
Lung | 0.48 ± 0.06 | 0.50 ± 0.15 |
Liver | 2.96 ± 0.34 | 3.48 ± 0.33 * |
Spleen | 0.18 ± 0.04 | 0.26 ± 0.05 |
Stomach | 0.76 ± 0.03 | 0.73 ± 0.06 |
Kidney | 0.60 ± 0.07 | 0.76 ± 0.05 |
Testes | 1.73 ± 0.05 | 1.77 ± 0.28 |
Female rats | n = 5 | n = 5 |
Brain | 0.78 ± 0.10 | 0.69 ± 0.05 |
Heart | 0.40 ± 0.01 | 0.41 ± 0.03 |
Lung | 0.47 ± 0.12 | 0.62 ± 0.04 |
Liver | 2.83 ± 0.02 | 3.28 ± 0.25 * |
Spleen | 0.24 ± 0.04 | 0.26 ± 0.04 |
Stomach | 0.62 ± 0.01 | 0.54 ± 0.04 |
Kidney | 0.66 ± 0.03 | 0.68 ± 0.01 |
Uterus | 0.47 ± 0.00 | 0.45 ± 0.06 |
Parameters | Control Group | Tocosh Flour Dose: 1000 mg/kg |
---|---|---|
Male rats | n = 5 | n = 5 |
AST (IU/L) | 113.00 ± 4.00 | 108.50 ± 1.50 |
ALT (IU/L) | 69.50 ± 3.50 | 70.00 ± 1.50 |
Alkaline Phosphatase (IU/L) | 231.00 ± 9.00 | 238.50 ± 0.50 |
Total Bilirubin (mg/dL) | 0.10 ± 0.00 | 0.10 ± 0.00 |
Total Protein (g/dL) | 6.95 ± 0.05 | 7.01 ± 0.05 |
Albumin (g/dL) | 3.80 ± 0.20 | 3.95 ± 0.05 |
Globulin (g/dL) | 3.15 ± 0.25 | 3.00 ± 0.10 |
Total cholesterol (mg/dL) | 59.50 ± 0.50 | 60.00 ± 0.00 |
Triglycerides (mg/dL) | 134.50 ± 8.50 | 107.00 ± 13.00 * |
HDL (mg/dL) | 12.50 ± 0.50 | 10.60 ± 0.40 |
LDL (mg/dL) | 20.00 ± 3.00 | 28.00 ± 3.00 * |
Glucose (mg/dL) | 100.50 ± 0.50 | 108.50 ± 1.50 |
Serum urea (mg/dL) | 37.50 ± 1.50 | 40.50 ± 2.50 |
Serum creatinine (mg/dL) | 0.44 ± 0.01 | 0.44 ± 0.03 |
Female rats | n = 5 | n = 5 |
AST (IU/L) | 116.50 ± 0.50 | 106.00 ± 0.50 |
ALT (IU/L) | 65.50 ± 0.50 | 63.00 ± 1.00 |
Alkaline Phosphatase (IU/L) | 235.50 ± 5.50 | 223.00 ± 17.00 |
Total Bilirubin (mg/dL) | 0.10 ± 0.00 | 0.10 ± 0.00 |
Total Protein (g/dL) | 6.90 ± 0.30 | 6.90 ± 0.20 |
Albumin (g/dL) | 3.80 ± 0.20 | 4.10 ± 0.00 |
Globulin (g/dL) | 3.05 ± 0.05 | 2.80 ± 0.20 |
Total cholesterol (mg/dL) | 57.00 ± 3.00 | 59.50 ± 0.50 |
Triglycerides (mg/dL) | 139.00 ± 1.00 | 130.50 ± 10.50 |
HDL (mg/dL) | 9.55 ± 0.25 | 8.25 ± 0.25 |
LDL (mg/dL) | 18.00 ± 2.00 | 25.00 ± 2.00 * |
Glucose (mg/dL) | 110.50 ± 3.50 | 113.00 ± 2.00 |
Serum urea (mg/dL) | 35.50 ± 2.50 | 34.00 ± 0.00 |
Serum creatinine (mg/dL) | 0.40 ± 0.02 | 0.46 ± 0.01 |
Parameters | Control Group | Tocosh Flour Dose: 1000 mg/kg |
---|---|---|
Male rats | n = 5 | n = 5 |
RBC (×106/mm3) | 7.09 ± 0.30 | 7.30 ± 0.08 |
White blood cells (×103/mm3) | 4.14 ± 0.13 | 3.91 ± 0.17 |
Hemoglobin (g/dL) | 14.70 ± 0.60 | 14.65 ± 0.15 |
Hematocrit (%) | 41.80 ± 1.80 | 43.55 ± 1.45 |
Eosinophils (%) | 1.50 ± 0.50 | 1.00 ± 0.00 |
Basophil (%) | 0.00 ± 0.00 | 0.00 ± 0.00 |
Monocytes (%) | 1.00 ± 0.00 | 2.00 ± 0.00 * |
Segmented (%) | 20.50 ± 8.50 | 17.00 ± 4.00 |
Lymphocytes (%) | 77.00 ± 9.00 | 80.50 ± 4.50 |
Platelets (×103/mm3) | 7.5 ± 0.26 | 7.22 ± 0.22 |
Female rats | n = 5 | n = 5 |
RBC (×106/mm3) | 7.00 ± 0.10 | 6.93 ± 0.22 |
White blood cells (×103/mm3) | 4.03 ± 0.18 | 4.20 ± 0.30 |
Hemoglobin (g/dL) | 14.65 ± 0.25 | 14.60 ± 0.10 |
Hematocrit (%) | 42.00 ± 0.00 | 41.50 ± 0.50 |
Eosinophils (%) | 0.00 ± 0.00 | 0.00 ± 0.00 |
Basophil (%) | 0.00 ± 0.00 | 0.00 ± 0.00 |
Monocytes (%) | 2.50 ± 0.50 | 1.50 ± 0.50 * |
Segmented (%) | 24.00 ± 1.00 | 17.00 ± 1.00 |
Lymphocytes (%) | 79.00 ± 1.00 | 80.50 ± 0.50 |
Platelets (×103/mm3) | 7.3 ± 0.20 | 7.6 ± 0.35 |
Compound | M.W. a | PSA b | n-Rot Bond (0–10) | n-ON (<10) c | n-OHNH d | Log Po/w e | LogKHSA f | Caco-2 g (nm/s) | App.MDCK (nm/s) h | % HIA i | % HOA j | Lipinski Rule of Five |
---|---|---|---|---|---|---|---|---|---|---|---|---|
α-chaconine | 852.070 | 199.560 | 15 | 15 | 8 | −0.091 | −0.875 | <25 poor | <25 poor | <25poor | Low | 3 |
α-solanine | 868.069 | 220.534 | 17 | 16 | 9 | −0.860 | −1.157 | <25 poor | <25 poor | <25poor | Low | 3 |
Solanidine | 397.643 | 22.288 | 1 | 2 | 1 | 5.007 | 0.554 | 1049 | 576 | 100 | High | 0 |
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Velasco-Chong, J.R.; Herrera-Calderón, O.; Rojas-Armas, J.P.; Hañari-Quispe, R.D.; Figueroa-Salvador, L.; Peña-Rojas, G.; Andía-Ayme, V.; Yuli-Posadas, R.Á.; Yepes-Perez, A.F.; Aguilar, C. TOCOSH FLOUR (Solanum tuberosum L.): A Toxicological Assessment of Traditional Peruvian Fermented Potatoes. Foods 2020, 9, 719. https://doi.org/10.3390/foods9060719
Velasco-Chong JR, Herrera-Calderón O, Rojas-Armas JP, Hañari-Quispe RD, Figueroa-Salvador L, Peña-Rojas G, Andía-Ayme V, Yuli-Posadas RÁ, Yepes-Perez AF, Aguilar C. TOCOSH FLOUR (Solanum tuberosum L.): A Toxicological Assessment of Traditional Peruvian Fermented Potatoes. Foods. 2020; 9(6):719. https://doi.org/10.3390/foods9060719
Chicago/Turabian StyleVelasco-Chong, Jonas Roberto, Oscar Herrera-Calderón, Juan Pedro Rojas-Armas, Renán Dilton Hañari-Quispe, Linder Figueroa-Salvador, Gilmar Peña-Rojas, Vidalina Andía-Ayme, Ricardo Ángel Yuli-Posadas, Andres F. Yepes-Perez, and Cristian Aguilar. 2020. "TOCOSH FLOUR (Solanum tuberosum L.): A Toxicological Assessment of Traditional Peruvian Fermented Potatoes" Foods 9, no. 6: 719. https://doi.org/10.3390/foods9060719