HEALTHLY PROPERTIES OF JERUSALEM ARTICHOKE FLOUR (HELIANTHUS TUBEROSUS L.)

Ewa Cieślik¹, Aneta Kopeć¹, Werner Praznik^2
1 Department of Human Nutrition, Agricultural University, Cracow, Poland
² Institute of Chemistry, University of Agricultural Sciences, Wien, Austria

ABSTRACT

The research was undertaken to determine the effect of Jerusalem artichoke’s tuber flour - “Jerusalem artichoke flour” on total cholesterol content, concentrations of HDL, LDL+VLDL lipoproteins and triglycerides in blood of experimental rats. The animals were divided into four experimental groups and fed for 24 days with mixtures containing various proportions of Jerusalem artichoke flour. On the last day of the experiment the rodents were anaesthetised and blood was sampled directly from the heart. Total cholesterol, HDL and triglycerides were assayed in blood serum. The content of LDL+ VLDL lipoproteins were calculated from the difference between total cholesterol and HDL lipoproteins. A declining tendency was observed for total cholesterol level and LDL+VLDL lipoproteins when the diet was supplemented with the Jerusalem artichoke flour. On the other hand the amount of triglycerides decreased statistically significantly in blood serum of animals fed diets with 10% and 15% supplement of Jerusalem artichoke flour.

Key words: Jerusalem artichoke flour, lipid profile, rats.

INTRODUCTION

Jerusalem artichoke (Helianthus tuberosus L.) also known as such choke belongs, as chicory and daisy to Compositae family (Asteriacae) [19].The plant originates from North America. It was first cultivated in Poland in the 18^th century as an ornamental and forage plant [18, 19]]. Jerusalem artichoke grows from 2 to 4 m high and has oval leaves, serrate-dentate, sharp on tops. Pollen baskets reaching 8 cm in diameter appear on sprout ends [1]. Tubers of various shapes and different skin colours form on the ends of underground stems or rootstocks [19].

Studies on nutritive value of Jerusalem artichoke tubers have revealed that they contain many important components [6, 9, 10, 24]. It was has been demonstrated that artichoke tubers have between 20.4 and 31.9% of dry matter, in which carbohydrates are the main component [4, 6]. The greatest part consists of water-soluble inulin and its concentrations range between 49.5 and 56.4% of dry matter, which constitutes about 11.3-14.2 g/100 g of fresh tuber mass [24]. Soluble carbohydrates present beside inulin are its derivatives – fructooligosaccharides, simple sugars (fructose and glucose) and saccharose. Beside soluble carbohydrates Jerusalem artichoke tubers contain also insoluble food cellulose fractions (cellulose and lignin), pectins and hemicelluloses (soluble cellulose fraction). Contents of these compounds in tubers depend mainly on a variety and fluctuate within a wide range of between 5.7 and 11.7% [6, 18].

Protein content in tubers of new Jerusalem artichoke cultivars, including Topsatr c.v., ranges between 0.8 and 1.4 g/100 of fresh mass [24]. Jerusalem artichoke protein contains all exogenic amino acids in very advantageous proportions [8]. Some authors have emphasized high vitamin content in artichoke tubers [27]. Among these the most frequently mentioned are vitamin C, β-carotene and B vitamins (thiamine, riboflavin, niacin and biotin). Moreover, Jerusalem artichoke tubers are characterized by high content of alkaligenously acting minerals, particularly potassium [7, 9]. The composition of artichoke tubers ash is comparable to potato tuber composition, however considerably higher amounts of potassium have been detected in Jerusalem artichoke tubers, between 63.4% [7] and 75.7% [14] in total ash content. Beside potassium also magnesium, calcium, sodium, iron, zinc and copper have been detected in its tuber ash [9]. Thrice higher concentrations of iron compounds in Jerusalem artichoke tubers than in potato are worthy of notice.

Due to high nutritive value and proportions of fructans (70-90%), and low content of toxic substances (lead, nitrates (III) and nitrates (V)) [7, 10] flour of Jerusalem artichoke tubers may be fully utilized as functional food supplement [5].

In the last ten years, interest in Jerusalem artichoke and potential utilisation of tubers for manufacturing functional food products has grown also in Poland [11, 24]. Research on new type of Jerusalem artichoke usability for fructose syrup production was conducted at the Agricultural University in Poznań [6]. Poznań based enterprise has started manufacturing a preparation of Jerusalem artichoke tubers under commercial name of Topinulin, now available in pharmacies and shops selling health foods.

Due to the fact that Jerusalem artichoke tubers are good source of fructans (fructooligosaccharides and inulin) they may positively decrease levels of some lipid fractions in organisms. During fructan fermentation in the small intestine short chain fatty acids form, which inhibit triglyceride and cholesterol synthesis in the liver. Fructan preparations (fructooligosaccharides and inulin) which are most frequently used for nutritive experiments on humans and animals are obtained from chicory roots. [11, 13, 15, 23, 29]. In the available literature only Varlamova et al [28] have attempted at determining the effect of Jerusalem artichoke tuber flour as a source of fructans upon total cholesterol concentrations in blood of rats, but did not assay individual lipid fractions.

Therefore, the studies were conducted to determine the effect of a Jerusalem artichoke tuber flour supplement to modified AIN-93G diet on body mass growth, lipid profile (total cholesterol, lipoproteins HDL, LDL+VLDL and triglycerides).

MATERIALS AND METHODS

Flour of Jerusalem artichoke tubers (Helianthus tuberosus L.) Topstar cv. collected in the spring 1999 (after wintering in soil). Jerusalem artichoke tubers were cultivated at the Experimental Station of Eggenburg Agricultural University situated in the northern part of Vienna. The level of basic components (proteins, saccharose, fiber and ash) were determinated in the Jerusalem artichoke flour with used analytical methods [2] and fructans with enzymatic method [16].

Experimental diets were prepared on the basis of AIN-93G diet [25]. The modification involved replacement of soybean oil with lard as a hypercholesterolemic factor. Due to high proportions of protein, saccharose, fiber and minerals in Jerusalem artichoke tuber flour, contents of these elements were balanced in the experimental mixtures (Table 1).

Experimental diets were prepared of corn starch (ICN, OH, USA) casein (95% N x 6,25, Sigma ST. Louis, MO,. USA), tert-butylhydroquinone (Sigma ST. Louis, MO,. USA) and vitamin and mineral mixtures (according to Reeves et al. 1993. Detailed experimental diets composition was presented in Table 2.

The experimental rats were obtained from the Department of Animal Nutrition, Institute of Animal Production in Cracow. They were albino males (Wistar rats), aged between 5-6 weeks with mean body weight 90-120 g. The studies were carried out in compliance with ethical requirements and were approved by the Local Ethical Commission. Animals were kept individually in metal cages in a room maintained at constant temperature and humidity, under 12 h/12 h light/dark cycle. During the adaptation period (7 days) the animals were fed commercial GLM-1 diet and drinking water ad libitum. After the adaptation period, the animals were randomly divided into four groups (six rats each) and fed four experimental diets (Table 2) providing graded levels of Jerusalem artichoke flour (0, 5, 10 and 15%) for 21 days. The rats had free access to water and food and the diet intake was controlled. The rats were weighed at the beginning and at the end of experimental periods. On the last day of the experimental periods, the rats which had been deprived of food overnight, were anesthetised by intraperitoneal injection of sodium thiopental (Biochemie, Vienna, Austria; 25 mg/100 g of body mass) and killed by withdrawing blood from the heart. Blood samples were collected to single tubes and centrifuged for 10 min at 4000 g to obtain blood serum.

The serum samples were analysed for total cholesterol (BioVendor kit No. 1085), HDL cholesterol (BioVendor kit No. 10855), and triglycerides (Bio Vendor kit No.12805). LDL + VLDL lipoprotein cholesterol level was calculated from the difference between total cholesterol and HDL cholesterol.

The data obtained were subjected to one-factorial analysis of variance and significance of differences between treatments was determined using Duncan multiple range test at P < 0.05 and P < 0.01. In addition, the relationships between increasing dietary fructan levels and serum lipids were described using linear regression analysis (Microsoft Excel, 1997).

RESULTS

In the nutritional experiment the diets were supplemented with 5%, 10% and 15% of “Jerusalem artichoke flour”. The diet consumption in individual experimental groups was 1506 g.

It was found that fructans in the Jerusalem artichoke flour may decrease the rate of body mass growth in rats. The highest body mass growth – 32.8 g was registered in group I, whereas the lowest – 21.8 g in group II, where the flour supplement was 5%. In groups II and IV the growths were respectively 28.8 g and 22.3 g (Table 3).

Jerusalem artichoke flour supplement caused a slight decline in total cholesterol level in the experimental animals’ blood serum. In group I total cholesterol was 2.63 mmol/L, the lowest content was registered in group III – 2.30 mmol/L, while in groups II and IV this fraction content remained on the same level – 2.50 mmol/L.

Concentrations of high density lipoproteins (HDL) in rat blood serum also revealed a declining tendency. The highest 2.07 mmol/l was noted in group I – control and the lowest in group III (1.82 mmol/l). In groups II and IV the concentrations were respectively 2.01 mmol/L and 2.06 mmol/L.

The contents of LDL+VLDL cholesterol, like high density lipoproteins, was decreasing slightly in the rodent blood. The highest level – 0.57mmol/L was detected in group I, while the lowest – 0.44 mmol/L in group IV. In groups II and III LDL+VLDL concentrations were respectively 0.49 mmol/L and 0.48 mmol/L.

Triglyceride level in animal blood serum from groups II and IV decreased statistically significantly in comparison with the control group. The lowest was registered in group III (0.34 mmol/L), while in group IV it was 0.44mmol/L. The changes were statistically significant in relation to the control group.

DISCUSSION

An analysis of the results obtained in the experiment where diets were supplemented with Jerusalem artichoke tuber flour revealed smaller body mass growths in experimental rats, and the lowest (by 34%) statistically significant growth was demonstrated in the group of animals fed the diet supplemented with 5% of the Jerusalem artichoke tuber flour. Such effect might have been due to accelerated intestine peristalsis, which weakened assimilability of nutrients (protein, mineral salts and vitamins) from the diets and lower energy density of the mixture (1 g of pure frutcooligosaccharide preparation supplies to the organism c.a. 1.5 kcal [26].

Available literature data do not corroborate obtained results. Varlamova et al. [28] did not register the effect of Jerusalem artichoke flour supplement on body mass growth in rats during a 3-month long experiment. On the other hand, in their 30-day experiment Kok et al. [21] observed body mass growth decreased by c.a. 12 g (in comparison with the control), in a group of rodents fed a diet with 10% supplement of short chain fructooligosaccharides.

Total blood serum cholesterol level in rats fed a diet with Jerusalem artichoke tuber flour supplement revealed a decreasing tendency, but the changes were statistically insignificant. The lowest cholesterol concentrations (2.30 mmol/L) were registered in blood serum of animals fed the experimental mixture with 10% Jerusalem artichoke flour supplement. It was by 12.5% lower in relation to the control group. Most probably propionic acid formed in result of fructan fermentation might have blocked cholesterol synthesis in the liver through inactivation of β-hydroxy, β-methylglutarilo-CoA and lowered total cholesterol level in some experimental groups. Moreover, pectins and hemicelluloses present in Jerusalem artichoke tuber flour [6] were binding exogenous cholesterol in the small intestine light. Soluble fraction of dietary fibre might have bound bile acids and so their synthesis from cholesterol in the liver increased. On the other hand in their nutritional experiment with rats, Varlamova et al. [28] found that total cholesterol level was decreasing with growing proportions of artichoke flour supplements in diets. It was the lowest in blood serum of rats fed a diet with 15% flour supplement. Yamaguchi et al. [29] obtained similar results in their experiment with rats in which they added a levan (branched fructan) to the experimental diets. The authors did not state precise cholesterol level in diet.

The lowest amount of blood serum HDL lipoproteins was registered in rats from group III in the experiment with Jerusalem artichoke flour. A decline in blood serum HDL in rodents from group III has been connected with decreased concentration of total cholesterol (Table 3). In group IV where artichoke flour supplement was 15%, HDL level grew advantageously to 2.06 mmol/L. There is no data in the available literature about the effect of Jerusalem artichoke flour on HDL cholesterol level. HDL lipoproteins prevent injuries of vascular endothelium, transport LDL + VLDL to the liver and thus decrease their quantity in blood. Moreover, high density lipoproteins protect LDL + VLDL against oxidative changes and atherogenic effect [20]. It has been also found that too low level of HDL lipoproteins (below 0.9 mmoml/L) does not have any protective properties towards the endothelium and does not prevent LDL + VLDL oxidation processes. HDL below 0.9 mmoml/L level may undergo oxidative changes and act as an atherogenic factor [22].

Blood serum level of LDL + VLDL lipoproteins in experimental rodents was decreasing with growing proportions of Jerusalem artichoke tuber flour in individual experiments.

The artichoke flour supplement to diets lowered low density lipoprotein level most, i.e. by 23%, in blood serum of rats in group IV in comparison to group I (Table 3). Despite the fact, analysis of variance and linear regression did not reveal statistically significant changes. A lack of significant differences might have been influenced by low number of animals per group (n = 6 thus high dispersion of results). A positive declining tendency of LDL + VLDL lipoproteins in rats’ blood serum might have been affected by many factors. Short chain fatty acids might have blocked total cholesterol synthesis in the liver. Total cholesterol binds to LDL + VLDL and is transported to various organism tissues. In result of decreased cholesterol production in the liver LDL + VLD synthesis might have been lower. The available world literature lacks data about the influence of Jerusalem artichoke flour on LDL + VLDL lipoprotein concentrations.

The analysis of variance revealed a significant decrease in triglyceride concentrations in blood serum of rats fed diets with 10% and 15% flour supplements. The lowest level of triglycerides was registered in group III (Table 3) - 32% decrease in comparison with the control group. A decline in blood serum triglyceride level might have been affected by accelerated intestine peristalsis, which made difficult digestion and absorption of fats. Hemicelluloses and pectins present in Jerusalem artichoke tubers might bind bile acids and thus make difficult the process of emulsification, digestion and absorption of triglycerides. Moreover, fructans are fermented by bifidobacteries in the colon and the products of this metabolism – short chain fatty acids, particularly propionic acid inhibit the enzymes of triaglycerol synthetase, which makes difficult resynthesis of triglycerids. It also affects a decreased content of free fatty acids through intensifying insulin sensitivity, which also influences decreased synthesis of triglycerides in the liver. The available literature lacks data about the effect of Jerusalem artichoke flour on triglyceride concentrations in organisms of people and experimental animals. Accessible data refer primarily to the effect of fructo-oligosaccharides on lipid metabolism. In their experiment on rats fed a diet with 19% FOS supplement Kok et al. [21] registered a decrease in blood serum TG level from 1.45 mmol/L to 0.87 mmol/L. On the other hand, in their experiment on rats Daubioul et al. [12] detected a declining tendency of blood serum TG in animals fed 10% FOS supplement.

CONCLUSIONS

Statistically significant decrease in rat body mass growths was demonstrated in the group of animals fed a diet with 5% supplement of Jerusalem artichoke flour. Blood serum total cholesterol level did not change significantly in rats from individual experimental groups. The content of LDL + VLDL lipoproteins revealed a declining tendency in animal blood serum of all experimental groups. Analysis of variance revealed significant decrease in blood serum triglyceride level in rats fed diets with 10 and 15% artichoke flour supplements.

Obtained results point to a potential of food enrichment with Jerusalem artichoke flour and purposefulness of further nutritional experiments with people to test the effect of Jerusalem artichoke tuber flour as a functional component of food upon lipid metabolism in organisms.

ACKNOWLEDGEMENTS

Supported by the State Committee for Scientific Research, project No. P06T 045 21.

REFERENCES

1. Anioł-Kwiatkowska J., 1994. Słonecznik bulwiasty to również roœlina lecznicza [Jerusalem artichoke is also a healing plant]. Wiad. Lek., 12, 12-13 [in Polish].

2. AOAC 1997. International, Association of Official Analytical Chemists, Official Methods of Analysis.

3. Barta J., 1993. Jerusalem artichoke as a multipurpose raw material for food products of high fructose or inulin content. Inulin and inulin containing Crops. Elsevier Science Publishers B.V., 323 - 338.

4. Barta J., Fodor P., Torok S., Vukov K., 1990. Mineral components and micro-elements in Jerusalem artichoke tubers grow in Hungary. Acta Alimen., 19, 41 - 46.

5. Berghofer E., Reiter E., 1997. Production and functional properties of Jerusalem artichoke powder. Carbohydrates as organic raw materials. IV WUV Universitätserlag, 153 - 161.

6. Chrapkowska K.J., Góral S., Piasecki M., 1993. Otrzymywanie syropów fruktozowych z bulw Helianthus tuberosus (topinambur) [Receiving a fructose syrup from Helianthus tuberosus tubers (Jeruslem artichoke)]. Mat. XXIV Ses. Nauk. KTiChŻ PAN, Wrocław, 161-164 [in Polish].

7. Cieœlik E., Baranowski M., 1997. Zawartoœć składników mineralnych i ołowiu w bulwach nowych odmian topinamburu (Helianthus tuberosus L.) [Minerals and lead content of Jerusalem artichoke new tubers]. Brom. Chem. Toksykol., 30, 66-67 [in Polish].

8. Cieœlik E., 1998. Amino acid content of Jerusalem artichoke (Helianthus tuberosus L.) tubers before and after storage in soil. Proc. Seven Semin. Inulin, Belgium, 86 - 87.

9. Cieœlik E., 1998. Zawartoœć składników mineralnych w bulwach nowych odmian topinamburu (Helianthus tuberosus L.) [Minerals content of Jerusalem artichoke new tubers]. Zesz. Nauk. AR Krak., 342, 10, 23 - 30 [in Polish].

10. Cieœlik E., Praznik W., Filipiak-Florkiewicz A., 1999. Correlation between the levels of nitrates, nitrites and vitamin C in Jerusalem artichoke tubers. Scand. J. Nutr., 49 S.

11. Daubiuoul C., Rousseau N., Demeure R., Gallez B., Taper H., Declerck B., Delzenne N., 2002. Dietary fructans, but not cellulose decrease triglicyceride accumulation in the liver of obese zucker fa/fa rats. J. Nutr., 132, 967 - 973.

12. Daubioul C., Taper H. S., Laurent De Wispelaere D., Delzenne N.M., 2000. Dietary oligofructose lessens hepatic steatiosis, but does not prevent hypertriglycerylemia in obese zucker rats. J. Nutr., 130, 1314 - 1319.

13. Delzenne N. M., 1999. The hypolipidemic effect of inulin: when animal studies help to approach the human problem. B. J. Nutr., 82, 3-4.

14. Delzenne N. M., Kok N. N., 1999. Biochemical basis of oligofructose-induced hypolipidemia in animal models. J. Nutr., 129, 3, 1467 S - 1469 S.

15. Delzenne N. M., Kok N. N., 2001. Effects of fructans-type prebiotics on lipid metabolism. Am. J. Clin. Nutr., 73, 456 S – 458 S.

16. Filipiak–Florkiewicz A., 2001. Wartoœć odżywcza bulw nowych odmian topinamburu (Heliantus tubeosus L.) oraz możliwoœci ich wykorzystania do produkcji chleba [The nutrition value of Jerusalem artichoke new tubers and possibilities of use in bread production]. Diss., AR Cracow [in Polish].

17. Filipiak-Florkiewicz A., Cieœlik E., 2001. Ocena sensoryczna pieczywa z różnym dodatkiem fruktanów [The sensory valuation of bakings with various addition of fructans]. Żyw. Człow. Met., Supl., 567-570.

18. Góral S., 1996. Topinambur - słonecznik bulwiasty - Helianthus tuberosus L. Nowe roœliny uprawne na cele spożywcze, przemysłowe i jako odnawialne Ÿródła energii. Jerusalem artichoke –tuber sunflower - Helianthus tuberosus L [Possibility of using new generation plants in food production, industry and in new alternative energy sources]. SGGW, Warsaw, 76 - 86.

19. Góral S., 1998. Zmiennoœć morfologiczna i plonowanie wybranych klonów słonecznika bulwiastego - topinamburu (Helianthus tuberosus L.) [Morfological variability and harvesting selected type of Jerusalem artichoke (Helianthus tuberosus L.)]. Hod. Roœl. Nasien., 2, 6 - 11.

20. Iskra M., Pioruńska-Stolzmann M., 2001. Przeciwutleniajšce właœciwoœci lipoprotein o wysokiej gęstoœci i ich zmiana w reakcji ostrej fazy [Antioxidant properties of high density lipoprotein and their change in acute phase reaction]. Risk Factors, 3 - 4, 11 - 18.

21. Kok N. N, Roberfroid M., Delzenne N., 1998. Systemic effects of non digestible fructooligosaccharides in rats. Functional properties of non-digestible carbohydrates. INRA Nantes, 123-125.

22. Nofer J. R., Von Eckardstein A., Kehrel B., 2000. Poza odwrotnym transportem cholesterolu. Plejotropowe mechanizmy antyaterogennego działania HDL [Besides inverted transport of cholesterol. Pleiotropic mechanismes of antyatherogenic properties of HDL]. Risk Factors, 2 - 3, 5 - 17.

23. Olson B., Schneeman O., 1998. Alimentary lipemia is enhanced in fiber- fed rats. J. Nutr, 128, 1031 - 1036.

24. Praznik W., Cieœlik E., Filipiak A., 1998. The influence of harvest time on the content of nutritional components in tubers of Jerusalem artichoke (Helianthus tuberosus L.). Proc. Seven Semin. Inulin, Belgium, 154 - 157.

25. Reeves P. G., Forrest H., Nielsen H., Fahey G. C., 1993. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing commitete on the reformulation of the AIN-76A rodent diet. J. Nutr., 123, 1939 - 1951.

26. Roberfroid M. B., 1999. Caloric value of inulin and oligofructose. J. Nutr., 129, 3, 1436 S – 1437 S.

27. Van Loo J, Coussement P., De Leenheer L., Hoebregs H., Smits G., 1995. On the presence of inulin and oligofructose as natural ingrediens in the western diet. Crit. Rev. in Food Scien. and Nutr., 36(6), 525 - 552.

28. Varlamova K., Partskhaladze E., Olshamovsky V., Danilova E., 1996. Potential uses of Jerusalem atrichoke tuber concentraties as food additives and prophylactics. Sixth Semin. Inuli, Braunschweig, Germany, 141 - 144.

29. Yamaguchi H., Hayashibara Y., Yamamoto Y., Iizuka M., Minamiura N., 2000. Hypolipidemic efects of hight-molecular and low-molecular levan in rats. Fourth Int. Fructans Symp., Arolla – Switzerland, 8. 11.

Responses to this article, comments are invited and should be submitted within three months of the publication of the article. If accepted for publication, they will be published in the chapter headed 'Discussions' and hyperlinked to the article.