Dose-Response Relationship between Dietary Polyphenols from Acorns and Parotid Gland Hypertrophy in Pigs


Proline contents of parotid glands (PG) in pigs constantly increase after the inclusion of different amounts of ripe hulled acorns in the diet providing high polyphenols levels. The dose-response relationship was estimated on natural hydrolizable tannins (expressed as tannic acid equivalent TAE) amounts of 25.8 to 36.1 g TAE/kg DM in experimental diets. Macroscopic and histological morphometry of parotid glands greatly varied according to feed intake and dosages of TAE ingested. The PG response (hypertrophy grade) on acorns’ tannins content in the diet was positively correlated (R2 = 0.748): the response to the protein precipitating activity (PPA) of tannins consisted of a functional parotidomegaly (hypertrophy), 1.34 up to 3.55 folds than control PGs, following an oral dosage 0.596 up 1.72 TAE g·kg body weight·d-1 respectively, after one week exposure.

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M. Cappai, P. Wolf, W. Pinna and J. Kamphues, "Dose-Response Relationship between Dietary Polyphenols from Acorns and Parotid Gland Hypertrophy in Pigs," Food and Nutrition Sciences, Vol. 3 No. 9, 2012, pp. 1261-1268. doi: 10.4236/fns.2012.39166.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] H. H. Dukes, “Prehension, Mastication, Salivary Secretion, Deglutition,” In: H. H. Dukes, Ed., The Physiology of Domestic Animals, 7th Edition, Comstock Publishing Associate, Ithaca, 1955, pp. 303-321.
[2] J. E. Beart, T. H. Lilley and E. Haslam, “Plant Polyphenols—Secondary Metabolism and Chemical Defence: Some Observations,” Phytochemistry, Vol. 24, 1985, pp. 33-38. doi:10.1016/S0031-9422(00)80802-X
[3] K. W. Tipton, E. H. Floyd, J. G. Marshall and J. B. McDevitt, “Resistance of Certain Grain Sorghum Hybrids to Bird Damage in Louisiana,” Agronomy Journal, Vol. 62, No. 2, 1970, pp. 211-213. doi:10.2134/agronj1970.00021962006200020010x
[4] R. W. Bullard, J. O. York and S. R. Kilburn, “Polyphenolic Changes in Ripening Bird-Resistant Sorghum,” Journal of Agricultural and Food Chemistry, Vol. 29, No. 5, 1981, pp. 973-981. doi:10.1021/jf00107a022
[5] D. L. Dreyer, J. C. Reese and K. C. Jones, “Aphid Feeding Deterrents in Sorghum. Bioassay, Isolation and Characterization,” Journal of Chemical Ecology, Vol. 7, No. 2, 1981, pp. 273-284. doi:10.1007/BF00995750
[6] H. B. Harris and R. E. Burns, “Relationship between Tannin Content of Sorghum Grain and Preharvest Seed Molding,” Agronomy Journal, Vol. 65, No. 6, 1973, pp. 957-959. doi:10.2134/agronj1973.00021962006500060033x
[7] Y. Henis, H. Tagari and R. Volcani, “Effect of Water Extracts of Carob Pods, Tannic Acid, and Their Derivatives on the Morphology and Growth of Microorganisms,” Applied Microbiology, Vol. 12, 1964, pp. 204-209.
[8] Y. A. Geidarn, A. G. Ambali and P. A. Onyeyili, “Preliminary Phytochemical and Antibacterial Evaluation of Crude Aqueous Extract of Psidium guajava Leaf,” Journal of Applied Science, Vol. 7, No. 4, 2007, pp. 511-514.
[9] H. Akiyama, K. Fujii, O. Yamasaki, T. Oono and K. Iwatsuki, “Antibacterial Action of Several Tannins against Staphylococcus aureus”, Journal of Antimicrobial Chemotherapy, Vol. 48, 2001, pp. 487-491. doi:10.1093/jac/48.4.487
[10] R. E. Benoit and R. Starkey, “Enzyme Inactivation as a Factor in the Inhibition of Decomposition of Organic Matter by Tannins,” Soil Science, Vol. 105, 1968, pp. 203-208. doi:10.1097/00010694-196804000-00001
[11] A. R. Collins, “Assays for Oxidative Stress and Antioxidant Status: Applications to Research into the Biological Effectiveness of Polyphenols,” American Journal of Clinical Nutrition, Vol. 81, 2005, pp. 261-267.
[12] A. Scalbert, I. T. Johnson and M. Saltmarsh, “Polyphenols: Antioxidants and beyond,” American Journal of Clinical Nutrition, Vol. 81, 2005, pp. 215-217.
[13] C. L. Keen, R. R. Holt, P. I. Oteiza, C. G. Fraga and H. H. Schmitz, “Cocoa Antioxidants and Cardiovascular Health,” American Journal of Clinical Nutrition, Vol. 81, 2005, pp. 298-303.
[14] M. Baumann and W. Muller, “The Effects of Tannin Containing Plants on Pathogenic Microorganisms,” Tier?rztl Umsch, Vol. 48, 1993, pp. 738-741.
[15] S. A. Sotohy, W. Muller and A. A. Ismail, “In Vitro Effect of Egyptian Tannin-Containing Plants and Their Extracts on the Survival of Pathogenic Bacteria,” Dtsch Tierarztl Wochenschr, Vol. 102, 1995, pp. 344-348.
[16] K. Funatogawa, S. Hayashi, H. Shimomura, T. Yoshida, T. Hatano, H. Ito and Y. Hirai, “Antibacterial Activity of Hydrolyzable Tannins Derived from Medicinal Plants against Helicobacter pylori,” Microbiology and Immunology, Vol. 48, 2004, pp. 251-261.
[17] A. H. Smith and R. I. Mackie, “Effect of Condensed Tannins on Bacterial Diversity and Metabolic Activity in the Rat Gastrointestinal Tract,” Applied and Environmental Microbiology, Vol. 70, 2004, pp. 1104-1115. doi:10.1128/AEM.70.2.1104-1115.2004
[18] T. Taguri, T. Tanaka and I. Kouno, “Antimicrobial Activity of 10 Different Plant Polyphenols against Bacteria Causing Food-Borne Disease,” Biological & Pharmaceutical Bulletin, Vol. 27, 2004, pp. 1965-1969. doi:10.1248/bpb.27.1965
[19] R. Puupponen-Pimi?, L. Nohynek, S. Hartmann-Schmidlin, M. K?hk?nen, M. Heinonen, K. M??tt?-Riihinen and K. M. Oksman-Caldentey, “Berry Phenolics Selectively Inhibit the Growth of Intestinal Pathogens,” Journal of Applied Microbiology, Vol. 98, 2005, pp. 991-1000. doi:10.1111/j.1365-2672.2005.02547.x
[20] A. Van Parys, F. Boyen, J. Dewulf, F. Haesbrouck and F. Pasmans, “The Use of Tannins to Control Salmonella Typhimurium Infections in Pigs,” Zoonoses Public Health, Vol. 57, No. 6, 2010, pp. 423-428. doi:10.1111/j.1863-2378.2009.01242.x
[21] B. R. Min and S. P. Hart, “Tannins for Suppression of Internal Parasites,” Journal of Animal Science, Vol. 81, 2003, pp. 102-109.
[22] S. Maity, J. R. Vedasiromoni and D. K. Ganguly, “AntiUlcer Effect of the Hot Water Extract of Black Tea (Camelia sinensis),” Journal of Ethnopharmacology, Vol. 46, 1995, pp. 167-174. doi:10.1016/0378-8741(95)01245-9
[23] F. Borrelli and A. A. Izzo, “The Plant Kingdom as a Source of Anti-Ulcer Remedies,” Phytotherapy Research, Vol. 14, 2000, pp. 581-591. doi:10.1002/1099-1573(200012)14:8<581::AID-PTR776>3.0.CO;2-S
[24] L. M. Sànchez Perera, D. Ruedas and B. C. Gòmez, “Gastric Antiulcer Effect of Rhizophora mangle L.,” Journal of Ethnopharmacology, Vol. 77, 2001, pp. 1-3. doi:10.1016/S0378-8741(01)00277-X
[25] S. Das, R. Prakash and S. N. Devaraj, “Antidiarrhoeal Effects of Methanolic Root Extract of Hemidesmus indicus (Indian Sarsaparilla)—An In Vitro and In Vivo Study,” Indian Journal of Experimental Biology, Vol. 41, 2003, pp. 363-366.
[26] T. Okuda, K. Mori and H. Hayatsu, “Inhibitory Effect of Tannins on Direct-Acting Mutagens,” Chemical & Pharmaceutical Bulletin, Vol. 32, 1984, pp. 3755-3758. doi:10.1248/cpb.32.3755
[27] Z. Y. Wang, S. J. Cheng, Z. C. Zhou, M. Athar, W. A. Khana, D. R. Bickers and H. Mukhtar, “Antimutagenic Activity of Green Tea Polyphenols,” Mutation Research/ Genetic Toxicology, Vol. 223, 1989, pp. 273-285.
[28] H. Imanishi, Y. Sasaki, T. Ohta, M. Watanabe, T. Kato, and Y. Shirasu, “Tea Tannin Components Modify the Induction of Sister-Chromatid Exchanges and Chromosome Aberrations in Mutagen-Treated Cultured Mammalian Cells and Mice,” Mutation Research/Genetic Toxicology, Vol. 259, 1991, pp. 79-87.
[29] M. L. Kuo, K. C. Lee and J. K. Lin, “Genotoxicities of Nitropyrenes and Their Modulation by Apigenin, Tannic Acid, Ellagic Acid and Indole-3-Carbinol in the Salmonella and CHO Systems,” Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, Vol. 270, 1992, pp. 87-95.
[30] S. C. Chen and K. T. Chung, “Mutagenicity and Antimutagenicity Studies of Tannic Acid and Its Related Compounds,” Food and Chemical Toxicology, Vol. 38, 2000, pp. 1-5. doi:10.1016/S0278-6915(99)00114-3
[31] L. T. Wu, C. C. Chu, J. G. Chung, C. H. Chen, L. S. Hsu and J. K. Liu, “Effects of Tannic Acid and Its Related Compounds on Food Mutagens or Hydrogen PeroxideInduced DNA Strand Breaks in Human Lymphocytes,” Mutation Research, Vol. 556, 2004, pp. 75-82. doi:10.1016/j.mrfmmm.2004.07.004
[32] H. Szaefer, M. Cichocki, D. Brauze and W. BaerDubowska, “Alteration in Phases I and II Enzyme Activities and Polycyclic Aromatic Hydrocarbons-DNA Adduct Formation by Plant Phenolics in Mouse Epidermis,” Nutrition and Cancer, Vol. 48, 2004, pp. 70-77. doi:10.1207/s15327914nc4801_10
[33] H. Szaefer, J. Kaczmarek, M. Rybczyńska, W. BaerDubowskaa, “The Effect of Plant Phenols on the Expression and Activity of Phorbol Ester-Induced PKC in Mouse Epidermis,” Toxicology, Vol. 230, 2007, pp. 1-10. doi:10.1016/j.tox.2006.10.001
[34] G. Galati and P. J. O’Brien, “Potential Toxicity of Flavonoids and Other Dietary Phenolics: Significance for Their Chemopreventive and Anticancer Properties,” Free Radical Biology & Medicine, Vol. 37, 2004, pp. 287-303. doi:10.1016/j.freeradbiomed.2004.04.034
[35] M. Matsuyama, T. Nakamura, H. Suzuki and T. Nagayo, “Morphogenesis of Duodenal Adenocarcinoma Induced by N-ethyl-N’-nitro-N-nitrosoguanidine in Mice and Rats,” Gann Monograph on Cancer Research, Vol. 17, 1975, pp. 269-281.
[36] S. Yoshizawa, T. Horiuchi, H. Fujiki, T. Yoshida, T. Okuda and T. Sugimura, “Antitumor Promoting Activity of (-)Epigallocatechin Gallate, the Main Constituent of Tannins in Green Tea,” Phytotherapy Research, Vol. 1, 1987, pp. 44-47. doi:10.1002/ptr.2650010110
[37] H. Mukhtar, M. Das, W. A. Khan, Z. Y. Wang, D. P. Bik and D. R. Bickers, “Exceptional Activity of Tannic Acid among Naturally Occurring Plant Phenols in Protecting against 7,12-dimethylbenz(a)anthracene-, benzo(a)pyrene-, 3-methylcholanthrene-, and tv-methyl-tv-nitrosourea-induced Skin Tumorigenesis in Mice,” Cancer Research, Vol. 48, 1988, pp. 2361-2365.
[38] Y. Fujita, T.Yamane, M. Tanaka, K. Kuwata, J. Okuzumi, T. Takahashi, H. Fujiki and T. Okuda, “Inhibitory Effect of (-)Epigallocatechin Galle on Carcinogenesis with N-ethyl-N’-nitro-N-nitrosoguanidine in Mouse Duodenum,” Japanese Journal of Cancer Research, Vol. 80, 1989, pp. 503-505. doi:10.1111/j.1349-7006.1989.tb01666.x
[39] L. L. Yang, C. Y. Lee and K. Y. Yen, “Induction of Apoptosis by Hydrolyzable Tannins from Eugenia jambos L. on Human Leukemia Cells,” Cancer Letters, Vol. 157, 2000, pp. 65-75. doi:10.1016/S0304-3835(00)00477-8
[40] S. Nam, D. M. Smith and Q. P. Dou, “Tannic Acid Potently Inhibits Tumor Cell Proteasome Activity, Increases p27 and Bax Expression, and Induces G1 Arrest and Apoptosis1,” Cancer Epidemiology, Biomarkers & Prevention, Vol. 10, 2001, pp. 1083-1088.
[41] D. B. Wells, H. D. Humphrey and J. J. Coll, “Relation of Tannic Acid to Liver Necrosis Occurring in Burns,” New England Journal of Medicine, Vol. 226, 1942, pp. 629-636. doi:10.1056/NEJM194204162261601
[42] B. Korpassy, “Tannins as Hepatic Carcinogens,” Progress in Experimental Tumor Research, Vol. 2, 1981, pp. 245-290.
[43] J. A. Neser, J. A. Coetzer, J. Boomker and H.Cable, “Oak (Quercus rubor) Poisoning in Cattle”, Journal of South African Veterinary Association, Vol. 53, 1982, pp. 151-155.
[44] T. F. Warner and E. A. Azen, “Tannins, Salivary ProlineRich Proteins and Oesophageal Cancer”, Medical Hypothesis, Vol. 26, 1988, pp. 99-102. doi:10.1016/0306-9877(88)90060-6
[45] B. W. Cousins, T. D. Tanksley Jr., D. A. Knabe and T. Zebrowska, “Nutrient Digestibility and Performance of Pigs Fed Sorghum Varying in Tannins Concentration,” Journal of Animal Science, Vol. 53, 1981, pp. 1534-1537.
[46] H. Mehansho, L. Butler and D. M. Carlson, “Dietary tannins and Salivary Proline Rich Proteins: Interactions, Induction, and Defense Mechanism,” Annual Review of Nutrition, Vol. 7, 1987, pp. 423-440. doi:10.1146/
[47] A. J. M. Jansman, “Tannins in Faba Beans (Vicia faba L.): Antinutritional Properties in Monogastric Animals,” Ph.D. Dissertation, Wageningen University, Wageningen, 1993.
[48] R. Lizardo, J. Peiniau and A. Aumaitre, “Effects of Sorghum on Performance, Digestibility of Dietary Components and Activities of Pancreatic and Intestinal Enzymes in the Weaned Piglets,” Animal Feed Science and Technology, Vol. 56, 1995, pp. 67-82. doi:10.1016/0377-8401(95)00813-3
[49] A. Schiavone, K. Guo, S. Tassone, L. Gasco Hernandez, E. R. Denti and I. Zoccarato, “Effects of Natural Extract of Chestnut Wood on Digestibility, Performance Traits and Nitrogen Balance of Broiler Chicks,” Poultry Science, Vol. 87, 2008, pp. 521-527. doi:10.3382/ps.2007-00113
[50] T. Shimada and T. Saioth, “Negative Effects of Acorns on the Wood Mouse Apodemus speciosus,” Researches on Population Ecology, Vol. 45, 2003, pp. 7-17.
[51] T. Takahashi and T. Shimada, “Selective Consumption of Acorns by the Japanese Wood Mouse according to Tannin Content: A Behavioral Countermeasure against Plant Secondary Metabolites,” Ecological Research, Vol. 23, 2008, pp. 1033-1038. doi:10.1007/s11284-008-0473-5
[52] A. Bennick, “Salivary Proline-Rich Proteins,” Molecular and Cellular Biochemistry, Vol. 45, 1982, pp. 83-99. doi:10.1007/BF00223503
[53] P. J. Austin, L. A. Suchar, C. T. Robbins and A. E. Hagerman, “Tannin Binding Proteins in Saliva of Deer and Their Absence in Saliva of Sheep and Cattle,” Journal of Chemical Ecology, Vol. 15, 1989, pp. 1335-1347. doi:10.1007/BF01014834
[54] C. McArthur, G. D. Sanson and A. M. Beal, “Salivary Proline-Rich Proteins in Mammals: Roles in Oral Homeostasis and Counteracting Dietary Tannin,” Journal of Chemistry Ecology, Vol. 21, 1995, pp. 663-691. doi:10.1007/BF02033455
[55] M. G. Cappai, P. Wolf, V. Grosse-Liesner, A. Kastner, G. Nieddu, W. Pinna and J. Kamphues, “Effect of Whole Acorns (Quercus pubescens) Shred Based Diet on Parotid Gland in Growing Pigs in Relation to Tannins,” Livestock Science, Vol. 134, 2010, pp. 183-186. doi:10.1016/j.livsci.2010.06.136
[56] M. Clauss, J. Gehrke, J.-M. Hatt, E. S. Dierenfeld, E. J. Flachm, R. Hermes, J. Castell, W. J. Streich and J. Fickel, “Tannin-Binding Salivary Proteins in Three captive Rhinoceros Species,” Comparative Biochemistry and Physiology, Vol. 140, 2005, pp. 67-72. doi:10.1016/j.cbpb.2004.11.005
[57] P. R. Astatt and T. Ingram, “Adaptation to Oak and Other Fibrous, Phenolic-Rich Foliage by a Small Mammal, Neotoma fuscipes,” Oecologia, Vol. 60, 1983, pp. 135-142. doi:10.1007/BF00379333
[58] C. Naumann and R. Bassler, “Die Chemische Untersuchung von Futtermitteln (Chemical Analysis of Animal Feed),” VDLUFA-Verlag, Darmstadt, 2004.
[59] P. G. Waterman and S. Mole, “Analysis of Plant Metabolites,” In: P. G. Waterman and S. Mole, Eds., Methods in Ecology Series, Blackwell Scientific Publications, Oxford, 1994.
[60] S. Betscher, A. Beineke, S. Hansen, A. M??eler, S. Kleinschmidt and J. Kamphues, “Type of Mucus Produced in Salivary Glands of Young Pigs Fed Diets of Different Physical Form (Grinding Intensity, Meal/Pellets),” Proceedings of the 14th Congress of the European Society of Veterinary and Comparative Nutrition, Zürich, 6-8 September 2010, p. 46.
[61] S. Betscher, A. Beineke, L. Sch?nfeld and J. Kamphues, “Effects of Diet’s Physical Form (Grinding Intensity; Meal/Pellets) on Morphological and Histological Parameters (e.g. Ratio of Neutral to Acid Mucins) of the Gastrointestinal Tract in Weaned Piglets,” Livestock Science, Vol. 134, 2010, pp. 149-151. doi:10.1016/j.livsci.2010.06.122
[62] J. Kamphues, V. Grosse-Liesner, S. Betscher, A. M?sseler, P. Wolf, M. Wintermann, S. Hansen and A. Beineke, “Saliva and Oesophageal Secretion—“Missing Links” in the Pathogenesis of Gastric Ulcers in Pigs?” Proceedings of the 13th Congress of the European Society of Veterinary and Comparative Nutrition, Oristano, 15-17 October 2009, p. 43.
[63] H. Mehansho, S. Clement, B. T. Sheares, S. Smith and D. M. Carlson, “Induction of Proline-Rich Glycoprotein Synthesis in Mouse Salivary Glands by Isoproterenol and by Tannins,” The Journal of Biological Chemistry, Vol. 260, 1985, pp. 4418-4423.
[64] D. K. Ann, S. Clements, E. M. Johnstones and D. M. Carlson, “Induction of Tissue-Specific Proline-Rich Protein Multigene Families in Rat and Mouse Parotid Glands by Isoproterenol,” The Journal of Biological Chemistry, Vol. 262, 1987, pp. 899-904.
[65] W. Pinna, M. G. Cappai, G. Moniello and G. Nieddu, “Tannins Concentration and Ultrastructural Peculiarities of Starch Granules in Acorns of Quercus Ilex L., Quercus Pubescens Willdenow and Quercus Suber L.,” Proceedings of the 11th Congress of the European Society of Veterinary and Comparative Nutrition, Leipzig, 1-3 November, 2007, p. 96.
[66] R. M. Holman and W. W. Robbins, “A Textbook of General Botany,” Wiley and Sons, Inc., New York, 1944.
[67] D. A. Bainbridge, “Symposium on Multiple-Use Management of California’s Hardwoods,” San Luis Obispo, California, 1986.
[68] T. Shimada and T. Saito, “Re-Evaluation of the Relationship between Rodent Populations and Acorn Masting: A Review from the Aspect of Nutrients and Defensive Chemicals in Acorns,” Population Ecology, Vol. 48, 2006, pp. 341-352. doi:10.1007/s10144-006-0012-6
[69] D. Tejerina, S. García-Torres, M. Cabeza de Vaca, F. M. Vázquez and R. Cava, “Acorns (Quercus rotundifolia Lam.) and Grass as Natural Sources of Antioxidants and Fatty Acids in the “Montanera” Feeding of Iberian Pig: Intraand Inter-Annual Variations,” Food Chemistry, Vol. 124, 2011, pp. 997-1004. doi:10.1016/j.foodchem.2010.07.058
[70] E. Cantòs, J. C. Espín, C. López-Bote, L. de la Hoz, J. A. Ordó?ez and F. A. Tomás-Barberán, “Phenolic Compounds and Fatty Acids from Acorns (Quercus spp.), the Main Dietary Constituent of Free-Ranged Iberian Pigs,” Journal of Agricultural and Food Chemistry, Vol. 51, 2003, pp. 6248-6255. doi:10.1021/jf030216v
[71] J. W. Hudson, “Preparation of Acorn Bread by Pomo Indians,” American Anthropologist, Vol. 2, 1900, pp. 775-776.
[72] H. E. Driver, “The Acorn in North American Indian Diet,” Proceedings of the Indiana Academy of Science, 1953, pp. 52-62.
[73] P. D. Goodrum, “Food of the Indians: Acorn Breads,” Pacific Historians, Vol. 17, 1973, pp. 77-80.
[74] G. W. Dimbleby, “Plants and Archaeology,” Paladin Books, St. Albans, 1978.
[75] D. A. Bainbridge, “Quercus, a Multi-Purpose Tree for Temperate Climates,” International Tree Crops Journal, Vol. 3, 1986, pp. 291-298. doi:10.1080/01435698.1986.9752800
[76] D. A. Bainbridge, “The Rise of Agriculture: A New Perspective,” Ambio, Vol. 14, No. 3, 1985, pp. 148-151.

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