The Polyamine Content in Various Foods on a Calorie Basis

Short Review

The Polyamine Content in Various Foods on a Calorie Basis

Corresponding authorDr. Kuniyasu Soda, Saitama Medical Center, Jichi Medical University, 1-847 Amanuma, Omiya, Saitama City, Saitama, 330-8503 Japan, Tel: +81-48-647-2111; Fax: +81-48-648-5188; 
Email: 
soda@jichi.ac.jp

Abstract
Background

The polyamines spermine and spermidine are synthesized from arginine and are found in almost all living cells. All diets comprised of cells of various types of living organisms and their associated substances thus contain polyamines, but in a wide variety of concentrations. Food polyamines are one of the important sources of body polyamines in mammals, as they have been found to be absorbed quickly from the intestinal lumen and distributed widely throughout the organs and tissues in the body. Blood polyamine levels are increased by an increase in polyamine intake and decreased by a restriction of food polyamine. Recent studies have shown that polyamines have a wide variety of biological activities. However, knowledge of the polyamine content in various foods is not complete.Design and Methods

In the present study, based on published reports, we have created a visual table of the polyamine content in foods on a calorie basis.Results

Bran and germs of cereals, vegetables, mushrooms, beans, and certain seafood’s and aged cheeses were defined as polyamine- rich foods per calorie. Polished cereals, dairy products except aged cheeses, the majority of seasonings, oils, deserts, and drinks including alcohol drinks contain little polyamine.Conclusions

The table that we created provides both the polyamine concentrations in various foods and important information for creating menus for the adjunctive treatment of various pathological conditions.

Keywords: Polyamine; Spermine; Spermidine; Diet; Food

Introduction

The polyamines spermine and spermidine are found in almost all cells. Because foods are comprised of various organisms and their associated products, almost all foods contain polyamines, but in a wide variety concentrations. Polyamines in the intestinal lumen are absorbed quickly and distributed throughout all organs and tissues [1-3]. Polyamines in foods are thus one of the important sources of polyamines in the body and the longterm and continuous intake of a polyamine-rich diet increases the polyamine concentrations in whole blood [4,5]. Conversely,  a restriction of polyamine intake with the inhibition of polyamine synthesis by suppressing the activities of enterobacteria by antimicrobial agents can decrease polyamine levels in the body [6,7].

Several studies showed that polyamines have many biological activities, including roles in membrane stability, signal transduction, and gene expression, and the protection of cells and DNA from harmful stimuli such as radiation, ultraviolet, singlet oxygen, superoxide, and anticancer drugs [8–16]. These roles underline the importance of food polyamines in human health and diseases. For example, the restriction of polyamine intake helps relieve the pain experienced by cancer patients, resulting in a better quality of life; it also slowed the growth of colon tumors in some conditions [17,18]. In the presence of spermine oxidase — the activities of which are observed in some pathological conditions such as Helicobacter pylori infection — increased polyamine intake (especially of spermine) may have deleterious effects on the stomach mucosa, because spermine oxidase degrades spermine to produce virulent substances such as aldehydes and hydrogen peroxides [19]. Contrarily, we showed that an increase in the polyamine concentration inhibited the age-associated or polyamine deficit-induced pro-inflammatory status and abnormal DNA methylation in mice. And a continuous and long-term increased polyamine intake gradually elevated blood spermine levels in humans and mice, and lifelong consumption of polyamine rich chow of which polyamine concentrations were about three times higher than those of soybeans suppressed age-associated pathologies and extended the lifespan of mice [5,20]. In the present study, we created a table providing the polyamine concentrations of various foods on a calorie basis as well as on a weight basis, for a better understanding of the polyamine concentrations in food.

Design and Methods

We collected the concentrations of spermine and spermidine in foods on a weight basis from published reports of the concentrations measured in European foods [21] and from those measured in Japanese foods [22,23]. When mean values were not described, intermediate values were employed.

The values for putrescine, a precursor of polyamines containing two amine residues, were omitted for the following reasons:(1) Putrescine is degraded in the intestinal lumen, and only a small percentage is absorbed. (2) Unlike other polyamines, the measurement of putrescine is often inaccurate because it creates a wide band in association with other neighboring substances when measured by high performance liquid chromatography (HPLC).

The polyamine contents on a calorie basis were obtained by dividing the polyamine content values on a weight basis by the food calorie per weight. We obtained the calories for the European foods from the Agricultural research service, nationalagricultural library, nutrient data laboratory (http:// ndb.nal.usda.gov/ndb/search/list), a calorie count (http://caloriecount.about.com/), and a French food composition table, Table Ciqual 2012 (http://www.afssa.fr/TableCIQUAL/). We obtained the calories for the Japanese foods from the Standard Tables of Food Composition in Japan, 2010 (ISBN9784915392870) published by Japan’s Ministry of Education, Culture, Sports, Science and Technology; the Council for Scienceand Technology (http://fooddb.jp/), and the website Eiyoukeisann. com (http://www.eiyoukeisan.com/dietary_logs/multi_edit_food). However, the calories of turban shell viscera and whelk viscera in the Nishimura et al. study [23] were notfound in these databases, and thus the calories of turban shells in Japanese food and whelk in western foods, respectively were used.

Results

The polyamine concentrations of various foods on a weight basis

The polyamine concentrations of various foods on a weight basis obtained in three studies [21-23] are shown in Figure 1. Our comparison of the polyamine concentrations in European foods with those in Japanese foods revealed that the concentrationswere similar to each other.

An examination of the polyamine contents on a weight basis revealed that bran and germ contain abundant polyamines,whereas polished grains contain little polyamines. These characteristics were also observed in breads, the concentrations of which were measured by Cipolla et al. [21], the polyamine concentrations of the whole grain breads were higher than those of white bread. Among vegetables and fruits, the polyamine concentrations of which were relatively low, some contained moderate amounts of polyamines: lettuce, broccoli, and corn. In contrast, beans, nuts, and mushrooms contained a large amount of polyamines. Fish meats and animal meats had relatively high polyamine concentrations on a weight basis. The polyamine concentrations in shellfishes were higher than those in fish meats.

One interesting findings was that the viscera of fishes, animals and roe contained extremely high polyamine concentrations on a weight basis. Among dairy products, although milk, cream, and butter contained little polyamines, cheeses (especially aged cheeses) contained a large amount of polyamines.
Figure 1
Seasonings, beverages and confectionaries generally contained little polyamines; exceptions were mustard (which is made ofplant seeds) and soy sauce and soybean paste (made of soybeans), all of which contained moderate amounts of polyamine.
Figure 2
The polyamine concentrations of various foods on a calorie basis

The polyamine concentrations of various foods on a calorie basis are shown in Figure 2, and numerical values used for Figure 1 are described in Table 1. On a calorie basis, bran and germ contain high amounts of polyamines, and polished rice grains have little polyamines. Although the polyamine contents in vegetables on a weight basis are low, those on a calorie basis aregenerally high because of the low calorie levels of vegetables. Unlike vegetables, fruits contain little polyamines on a caloriebasis, because of their high calorie per weight. Although the polyamine concentrations of nuts on a weight basis are high, they are relatively low on a calorie basis. Mushrooms contain the highest amount of polyamine among all of the foods examined,although the majority of the polyamine content is spermidine.
The very high content of polyamine in seafood’s on a weight basis is observed only in certain seafoods (Figure 2) such asoyster, short-neck clam and viscera of turban shell, and they also contain a large amount of polyamine on a calorie basis. The polyamine concentrations of fish meats on a calorie basis are not as high as those on a weight basis, similar to those in animal meats. Although animal viscera have a large amount of polyamine on a weight basis, their polyamine concentrations on a calorie basis are very low. Similarly, the high calorie levels of animal meats seemed to negate the moderate amount ofpolyamine in animal meats on a weight basis, and the polyamine concentrations of animal meats on a calorie basis were low.The majority of seasonings, beverages and confectionaries contain little polyamine, whereas mustard and soy sauce containmoderate amounts of polyamine even on a calorie basis.
*1 grilled, *2 Duc k liver paste, *3 Goose liver paste, *4 Liver paste, – : not measured
Polyamine concentrations on a calorie basis (nmol/kcal)Table 1. Polyamine concentrations on a calorie basis in various foods.
Discussion

Our study provided several findings of interest. First, there is a large difference in the polyamine concentrations of foods on a calorie basis and those on a weight basis. The polyamine-rich foods on a calorie basis are the bran and germ of grains, vegetables, beans, mushrooms, some shellfishes, and aged cheeses. Contrarily, polyamine-deficient foods on a calorie basis are polished cereals, the majority of dairy products except aged cheeses, the majority of seasonings, oil, deserts, and drinks including those with alcohol. The major differences in the polyamine contents of foods indicate that food preferences may greatly affect individual consumers’ polyamine intake in differing parts of the world. Indeed, we have shown that Japanese food, which is composed of many soybean products and seafood, is a polyamine-rich diet on a calorie basis [24]. Similarly, a Mediterranean diet composed of abundant vegetables, beans, and seafood is rich in polyamines on a calorie basis [25]. Second, polyamine concentrations differ greatly among different parts of foods; for example, germ and bran contain relatively large amounts of polyamines, whereas polished grains have few polyamines, and the viscera of seafood as well as animals and roe contain extremely large amounts of polyamines. Watanabe et al. showed that the polyamine concentrations in the rat differ significantly between organs and tissues, and rat muscle tissues have lower polyamine concentrations compared to viscera [26,27].The findings that polyamine concentrations in foods differ depending on the parts of the food indicate that the dietary pattern, i.e., whether only meat of seafood or seafood with viscera is preferred, may greatly affect an individual’s polyamine intake from food. A typical example is the traditional Japanese diet, which includes viscera and roe of seafood and viscera of animal meats. For example, tsukudani is a product of shrimp, shellfishes, and/or small fishes including viscera and roe boiled in soy sauce, kanroni is made of seafoods including viscera and roe stewed in soy sauce and sugar, tarako, mentaiko, ikura, andkazunoko are roe products, and horumon and motsu-ni are viscera including the broiled or boiled liver of animals.Third, fermentation seems to increase the concentrations of polyamines as well as those of other biogenic amines [28], andthis is typically observed in dairy products: although milk contains little polyamine, cheeses (especially aged cheeses) containlarge amounts of polyamines, especially spermidine.

Recent studies have brought to light the importance of food polyamines, not only as a source of polyamines in the body but also as substances that elicit many biological activities in the body. Our compilation of the polyamine concentrations of foods on a calorie basis as well as on a weight basis may contribute to food choices to address various diseases and health problems.

 References

  1. Bardocz S, Duguid TJ, Brown DS, Grant G, Pusztai A et al. The importance of dietary polyamines in cell regeneration and growth. Br J Nutr. 1995, 73(6): 819-828.
  2. Bardócz S, Grant G, Brown DS, Ralph A, Pusztai A. Polyamines in food—implications for growth and health. J Nutr Biochem. 1993, 4(2): 66-71.
  3. Bardocz S, Brown DS, Grant G, Pusztai A. Luminal and basolateral polyamine uptake by rat small intestine stimulated to grow by Phaseolus vulgaris lectin phytohaemagglutinin in vivo. Biochim Biophys Acta. 1990, 1034(1): 46-52.
  4. Soda K, Kano Y, Sakuragi M, Takao K, Lefor A et al. Long-term oral polyamine intake increases blood polyamine concentrations. J Nutr Sci Vitaminol (Tokyo). 2009, 55(4): 361-366.
  5. Soda K, Dobashi Y, Kano Y, Tsujinaka S, Konishi F. Polyamine-rich food decreases age-associated pathology and mortality in aged mice. Exp Gerontol. 2009, 44(11): 727-732.
  6. Sarhan S, Knodgen B, Seiler N. The gastrointestinal tract as polyamine source for tumor growth. Anticancer Res. 1989, 9(1): 215-223.
  7. Nishimura K, Araki N, Ohnishi Y, Kozaki S. Effects of dietary polyamine deficiency on Trypanosoma gambiense infection in rats. Exp Parasitol. 2001, 97(2): 95-101.
  8. Hochman J, Katz A, Bachrach U. Polyamines and protein kinase II. Effect of polyamines on cyclic AMP–dependent protein kinase from rat liver. Life Sci. 1978, 22(17): 1481-1484.
  9. Tabib A, Bachrach U. Activation of the proto-oncogene c-myc and c-fos by c-ras: involvement of polyamines. Biochem Biophys Res Commun. 1994, 202(2): 720-727.
  10. Panagiotidis CA, Artandi S, Calame K, Silverstein SJ. Polyamines alter sequence-specific DNA-protein interactions. Nucleic Acids Res. 1995, 23(10): 1800-1809.
  11. Childs AC, Mehta DJ, Gerner EW. Polyamine-dependent gene expression. Cell Mol Life Sci. 2003, 60(7): 1394-1406.
  12. Brune B, Hartzell P, Nicotera P, Orrenius S. Spermine prevents endonuclease activation and apoptosis in thymocytes. Exp Cell Res. 1991, 195(2): 323-329.
  13. Khan AU, Di Mascio P, Medeiros MH, Wilson T. Spermine and spermidine protection of plasmid DNA against single-strand breaks induced by singlet oxygen. Proc Natl Acad Sci U S A. 1992, 89(23): 11428-11430.
  14. Spotheim-Maurizot M, Ruiz S, Sabattier R, Charlier M. Radioprotection of DNA by polyamines. Int J Radiat Biol. 1995, 68(5): 571-577.
  15. Chiu S, Oleinick NL. Radioprotection of cellular chromatin by the polyamines spermine and putrescine: preferential action against formation of DNA-protein crosslinks. Radiat Res. 1998, 149(6): 543-549.
  16. Sy D, Hugot S, Savoye C, et al. Radioprotection of DNA by spermine: a molecular modelling approach. Int J Radiat Biol. 1999, 75(8): 953-961.
  17. Cipolla BG, Havouis R, Moulinoux JP. Polyamine reduced diet (PRD) nutrition therapy in hormone refractory prostate cancer patients. Biomed Pharmacother. 2010, 64(5): 363-368.
  18. Vargas AJ, Wertheim BC, Gerner EW, et al. Dietary polyamine intake and risk of colorectal adenomatous polyps. Am J Clin Nutr. 2012, 96(1): 133-141.
  19. Xu H, Chaturvedi R, Cheng Y, et al. Spermine oxidation induced by Helicobacter pylori results in apoptosis and DNA damage: implications for gastric carcinogenesis. Cancer Res. 2004, 64(23): 8521-8525.
  20. Soda K, Kano Y, Chiba F, Koizumi K, Miyaki Y. Increased polyamine intake inhibits age-associated alteration in global DNA methylation and 1,2-dimethylhydrazine-induced tumorigenesis. PLoS One. 2013, 8(5): e64357.
  21. Cipolla BG, Havouis R, Moulinoux JP. Polyamine contents in current foods: a basis for polyamine reduced diet and a study of its long term observance and tolerance in prostate carcinoma patients. Amino Acids. 2007, 33(2): 203-212.
  22. Nishibori N, Fujihara S, Akatuki T. Amounts of polyamines in foods in Japan and intake by Japanese. Food Chem. 2006, 100
  23. Nishimura K, Shiina R, Kashiwagi K, Igarashi K. Decrease in polyamines with aging and their ingestion from food and drink. J Biochem. 2006, 139(1): 81-90.
  24. Binh PNT, Soda K, Kawakami M. Gross domestic product and dietary pattern among 49 western countries with a focus on polyamine intake. Health. 2010, 2(11): 1327-1334.
  25. Binh PNT, Soda K, Kawakami M. Mediterranean diet and polyamine intake: possible contribution of increased polyamine intake to inhibition of age-associated disease. Nutrition and Dietary Supplements. 2011, 3: 1-7.
  26. Watanabe S, Sato S, Nagase S, Saito T. Therapeutic significance of the polyamine level in tissues of rats treated with adriamycin and cisplatin. Anticancer Drugs. 1996, 7(1): 114-120.
  27. Watanabe S, Sato S, Nagase S, Shimosato K, Ohkuma S. Effects of methotrexate and cyclophosphamide on polyamine levels in various tissues of rats. J Drug Target. 1999, 7(3): 197-205.
  28. Okamoto A, Sugi E, Koizumi Y, Yanagida F, Udaka S. Polyamine content of ordinary foodstuffs and various fermented foods. Biosci Biotechnol Biochem. 1997, 61(9): 1582-1584.

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