Pelargonidin 3-glucoside-enriched strawberry attenuates symptoms of DSS-induced inflammatory bowel disease and diet-induced metabolic syndrome in rats

European Journal of Nutrition volume 59, pages2905–2918(2020)Cite this article

Abstract

Purpose

To determine whether the anthocyanin, pelargonidin 3-glucoside (P3G), attenuates symptoms of inflammatory bowel disease (IBD) and metabolic syndrome in rats.

Methods

We tested P3G-enriched strawberry in two models of chronic inflammation in rats, chronic IBD induced by 0.5% dextran sodium sulphate in the drinking water for 12 weeks (D) and metabolic syndrome induced by a high-carbohydrate, high-fat diet (H) for 16 weeks. P3G-enriched strawberry was added to the diet for the final 6 weeks in IBD rats (DP) or 8 weeks in H rats (HP) to provide a dose of 8 mg P3G/kg/day.

Results

D rats had marked diarrhoea, bloody stools, erosion of mucosal epithelium, crypt atrophy, loss of villi and goblet cells, and inflammatory cell infiltration. These symptoms were reversed by P3G with healthy stools and mucosal lining of ileum and colon including increased villi, crypts and goblet cells and reduced inflammation. H rats developed hypertension, dyslipidaemia, central obesity, increased ventricular stiffness, cardiac and liver inflammation, and steatosis. P3G treatment in H rats improved systolic blood pressure, ventricular stiffness, and cardiac and liver structure, and reduced abdominal fat, abdominal circumference and body weight gain.

Conclusions

Our study indicates that dietary P3G decreased inflammation to decrease the symptoms of IBD, and to improve cardiovascular, liver and metabolic functions in metabolic syndrome.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. 1.

    Brown L, Poudyal H, Panchal SK (2015) Functional foods as potential therapeutic options for metabolic syndrome. Obes Rev 16(11):914–941. https://doi.org/10.1111/obr.12313

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Ghattamaneni NKR, Panchal SK, Brown L (2018) Nutraceuticals in rodent models as potential treatments for human Inflammatory Bowel Disease. Pharmacol Res 132:99–107. https://doi.org/10.1016/j.phrs.2018.04.015

    Article  PubMed  Google Scholar 

  3. 3.

    Wu GD (2014) Diet, the gut microbiome and the metabolome in IBD. Nestle Nutr Inst Workshop Ser 79:73–82. https://doi.org/10.1159/000360686

    Article  PubMed  Google Scholar 

  4. 4.

    Bernstein CN, Fried M, Krabshuis JH, Cohen H, Eliakim R, Fedail S, Gearry R, Goh KL, Hamid S, Khan AG, LeMair AW, Malfertheiner Ouyang Q, Rey JF, Sood A, Steinwurz F, Thomsen OO, Thomson A, Watermeyer G (2010) World Gastroenterology Organization practice guidelines for the diagnosis and management of IBD in 2010. Inflamm Bowel Dis 16(1):112–124. https://doi.org/10.1002/ibd.21048

    Article  PubMed  Google Scholar 

  5. 5.

    Samson SL, Garber AJ (2014) Metabolic syndrome. Endocrinol Metab Clin North Am 43(1):1–23. https://doi.org/10.1016/j.ecl.2013.09.009

    Article  PubMed  Google Scholar 

  6. 6.

    Naseri R, Farzaei F, Haratipour P, Nabavi SF, Habtemariam S, Farzaei MH, Khodarahmi R, Tewari D, Momtaz S (2018) Anthocyanins in the management of metabolic syndrome: a pharmacological and biopharmaceutical review. Front Pharmacol 9:1310. https://doi.org/10.3389/fphar.2018.01310

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Basu A, Nguyen A, Betts NM, Lyons TJ (2014) Strawberry as a functional food: an evidence-based review. Crit Rev Food Sci Nutr 54(6):790–806. https://doi.org/10.1080/10408398.2011.608174

    CAS  Article  PubMed  Google Scholar 

  8. 8.

    Afrin S, Gasparrini M, Forbes-Hernandez TY, Reboredo-Rodriguez P, Mezzetti B, Varela-Lopez A, Giampieri F, Battino M (2016) Promising health benefits of the strawberry: a focus on clinical studies. J Agric Food Chem 64(22):4435–4449. https://doi.org/10.1021/acs.jafc.6b00857

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Edirisinghe I, Burton-Freeman B, Varelis P, Kappagoda T (2008) Strawberry extract caused endothelium-dependent relaxation through the activation of PI3 kinase/Akt. J Agric Food Chem 56(20):9383–9390. https://doi.org/10.1021/jf801864t

    CAS  Article  PubMed  Google Scholar 

  10. 10.

    Vendrame S, Klimis-Zacas D (2015) Anti-inflammatory effect of anthocyanins via modulation of nuclear factor-κB and mitogen-activated protein kinase signaling cascades. Nutr Rev 73(6):348–358. https://doi.org/10.1093/nutrit/nuu066

    Article  PubMed  Google Scholar 

  11. 11.

    Fredericks CH, Fanning KJ, Gidley MJ, Netzel G, Zabaras D, Herrington M, Netzel M (2013) High-anthocyanin strawberries through cultivar selection. J Sci Food Agric 93(4):846–852. https://doi.org/10.1002/jsfa.5806

    CAS  Article  PubMed  Google Scholar 

  12. 12.

    Kanodia L, Borgohain M, Das S (2011) Effect of fruit extract of Fragaria vesca L. on experimentally induced inflammatory bowel disease in albino rats. Indian J Pharmacol 43(1):18–21. https://doi.org/10.4103/0253-7613.75660

    Article  PubMed  PubMed Central  Google Scholar 

  13. 13.

    Fang J (2015) Classification of fruits based on anthocyanin types and relevance to their health effects. Nutrition 31(11–12):1301–1306. https://doi.org/10.1016/j.nut.2015.04.015

    CAS  Article  PubMed  Google Scholar 

  14. 14.

    Sodagari HR, Farzaei MH, Bahramsoltani R, Abdolghaffari AH, Mahmoudi M, Rezaei N (2015) Dietary anthocyanins as a complementary medicinal approach for management of inflammatory bowel disease. Expert Rev Gastroenterol Hepatol 9(6):807–820. https://doi.org/10.1586/17474124.2015.1002086

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Fang J (2014) Bioavailability of anthocyanins. Drug Metab Rev 46(4):508–520. https://doi.org/10.3109/03602532.2014.978080

    CAS  Article  Google Scholar 

  16. 16.

    Ghattamaneni NKR, Panchal SK, Brown L (2019) Cyanidin 3-glucoside from Queen Garnet plums and purple carrots attenuates DSS-induced inflammatory bowel disease in rats. J Funct Foods 56:194–203. https://doi.org/10.1016/j.jff.2019.01.028

    CAS  Article  Google Scholar 

  17. 17.

    Bhaswant M, Fanning K, Netzel M, Mathai ML, Panchal SK, Brown L (2015) Cyanidin 3-glucoside improves diet-induced metabolic syndrome in rats. Pharmacol Res 102:208–217. https://doi.org/10.1016/j.phrs.2015.10.006

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Bhaswant M, Shafie SR, Mathai ML, Mouatt P, Brown L (2017) Anthocyanins in chokeberry and purple maize attenuate diet-induced metabolic syndrome in rats. Nutrition 41:24–31. https://doi.org/10.1016/j.nut.2016.12.009

    CAS  Article  PubMed  Google Scholar 

  19. 19.

    Ichiyanagi T, Kashiwada Y, Shida Y, Sekiya M, Hatano Y, Takaishi Y, Ikeshiro Y (2013) Structural elucidation and biological fate of two glucuronyl metabolites of pelargonidin 3-O-β-d-glucopyranoside in rats. J Agric Food Chem 61(3):569–578. https://doi.org/10.1021/jf3032793

    CAS  Article  PubMed  Google Scholar 

  20. 20.

    Ghattamaneni NKR, Panchal SK, Brown L (2018) An improved rat model for chronic inflammatory bowel disease. Pharmacol Rep 71(1):149–155. https://doi.org/10.1016/j.pharep.2018.10.006

    Article  PubMed  Google Scholar 

  21. 21.

    Giampieri F, Alvarez-Suarez JM, Battino M (2014) Strawberry and human health: effects beyond antioxidant activity. J Agric Food Chem 62(18):3867–3876. https://doi.org/10.1021/jf405455n

    CAS  Article  PubMed  Google Scholar 

  22. 22.

    Panchal SK, Poudyal H, Iyer A, Nazer R, Alam MA, Diwan V, Kauter K, Sernia C, Campbell F, Ward L, Gobe G, Fenning A, Brown L (2011) High-carbohydrate, high-fat diet-induced metabolic syndrome and cardiovascular remodeling in rats. J Cardiovasc Pharmacol 57(5):611–624. https://doi.org/10.1097/FJC.0b013e31821b1379

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Sekar S, Shafie SR, Prasadam I, Crawford R, Panchal SK, Brown L, Xiao Y (2017) Saturated fatty acids induce development of both metabolic syndrome and osteoarthritis in rats. Sci Rep 7:46457. https://doi.org/10.1038/srep46457

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. 24.

    John OD, Mouatt P, Prasadam I, Xiao Y, Panchal SK, Brown L (2019) The edible native Australian fruit, Davidson’s plum (Davidsonia pruriens), reduces symptoms in rats with diet-induced metabolic syndrome. J Funct Foods 56:204–215. https://doi.org/10.1016/j.jff.2019.03.018

    CAS  Article  Google Scholar 

  25. 25.

    Parlee SD, Lentz SI, Mori H, MacDougald OA (2014) Quantifying size and number of adipocytes in adipose tissue. Methods Enzymol 537:93–122. https://doi.org/10.1016/B978-0-12-411619-1.00006-9s

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Vasina V, Broccoli M, Ursino MG, Canistro D, Valgimigli L, Soleti A, Paolini M, De Ponti F (2010) Non-peptidyl low molecular weight radical scavenger IAC attenuates DSS-induced colitis in rats. World J Gastroenterol 16(29):3642–3650. https://doi.org/10.3748/wjg.v16.i29.3642

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. 27.

    Li D, Wang P, Luo Y, Zhao M, Chen F (2017) Health benefits of anthocyanins and molecular mechanisms: update from recent decade. Crit Rev Food Sci Nutr 57(8):1729–1741. https://doi.org/10.1080/10408398.2015.1030064

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Poudyal H, Panchal S, Brown L (2010) Comparison of purple carrot juice and β-carotene in a high-carbohydrate, high-fat diet-fed rat model of the metabolic syndrome. Br J Nutr 104(9):1322–1332. https://doi.org/10.1017/s0007114510002308

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Yan Y, Kolachala V, Dalmasso G, Nguyen H, Laroui H, Sitaraman SV, Merlin D (2009) Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS One 4(6):e6073. https://doi.org/10.1371/journal.pone.0006073

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Farzaei MH, Bahramsoltani R, Abdolghaffari AH, Sodagari HR, Esfahani SA, Rezaei N (2016) A mechanistic review on plant-derived natural compounds as dietary supplements for prevention of inflammatory bowel disease. Expert Rev Gastroenterol Hepatol 10(6):745–758. https://doi.org/10.1586/17474124.2016.1145546

    CAS  Article  PubMed  Google Scholar 

  31. 31.

    Alipour M, Zaidi D, Valcheva R, Jovel J, Martinez I, Sergi C, Walter J, Mason AL, Wong GK, Dieleman LA, Carroll MW, Huynh HQ, Wine E (2016) Mucosal barrier depletion and loss of bacterial diversity are primary abnormalities in paediatric ulcerative colitis. J Crohns Colitis 10(4):462–471. https://doi.org/10.1093/ecco-jcc/jjv223

    Article  PubMed  Google Scholar 

  32. 32.

    Moran CJ, Walters TD, Guo CH, Kugathasan S, Klein C, Turner D, Wolters VM, Bandsma RH, Mouzaki M, Zachos M, Langer JC, Cutz E, Benseler SM, Roifman CM, Silverberg MS, Griffiths AM, Snapper SB, Muise AM (2013) IL-10R polymorphisms are associated with very-early-onset ulcerative colitis. Inflamm Bowel Dis 19(1):115–123. https://doi.org/10.1002/ibd.22974

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Amini AM, Muzs K, Spencer JP, Yaqoob P (2017) Pelargonidin-3-O-glucoside and its metabolites have modest anti-inflammatory effects in human whole blood cultures. Nutr Res 46:88–95. https://doi.org/10.1016/j.nutres.2017.09.006

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  34. 34.

    Farzaei MH, El-Senduny FF, Momtaz S, Parvizi F, Iranpanah A, Tewari D, Naseri R, Abdolghaffari AH, Rezaei N (2018) An update on dietary consideration in inflammatory bowel disease: anthocyanins and more. Expert Rev Gastroenterol Hepatol 12(10):1007–1024. https://doi.org/10.1080/17474124.2018.1513322

    CAS  Article  PubMed  Google Scholar 

  35. 35.

    Yang G, Wang H, Kang Y, Zhu MJ (2014) Grape seed extract improves epithelial structure and suppresses inflammation in ileum of IL-10-deficient mice. Food Funct 5(10):2558–2563. https://doi.org/10.1039/c4fo00451e

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Pandurangan AK, Saadatdoust Z, Esa NM, Hamzah H, Ismail A (2015) Dietary cocoa protects against colitis-associated cancer by activating the Nrf2/Keap1 pathway. BioFactors 41(1):1–14. https://doi.org/10.1002/biof.1195

    CAS  Article  PubMed  Google Scholar 

  37. 37.

    Biagioli M, Carino A, Fiorucci C, Annunziato G, Marchiano S, Bordoni M, Roselli R, Giorgio CD, Castiglione F, Ricci P, Bruno A, Faccini A, Distrutti E, Baldoni M, Costantino G, Fiorucci S (2019) The aryl hydrocarbon receptor (AhR) mediates the counter-regulatory effects of pelargonidins in models of inflammation and metabolic dysfunctions. Nutrients 11(8):1820. https://doi.org/10.3390/nu11081820

    CAS  Article  PubMed Central  Google Scholar 

  38. 38.

    Putta S, Yarla NS, Kumar EK, Lakkappa DB, Kamal MA, Scotti L, Scotti MT, Ashraf GM, Barreto GE, Rao BSB, Kumari DS, Reddy GV, Tarasov VV, Imandi SB, Aliev G (2017) Preventive and therapeutic potentials of anthocyanins in diabetes and associated complications. Curr Med Chem 25(39):5347–5371. https://doi.org/10.2174/0929867325666171206101945

    CAS  Article  Google Scholar 

  39. 39.

    Petersen C, Bharat D, Cutler BR, Gholami S, Denetso C, Mueller JE, Cho JM, Kim JS, Symons JD, Anandh Babu PV (2018) Circulating metabolites of strawberry mediate reductions in vascular inflammation and endothelial dysfunction in db/db mice. Int J Cardiol 263:111–117. https://doi.org/10.1016/j.ijcard.2018.04.040

    Article  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Amani R, Moazen S, Shahbazian H, Ahmadi K, Jalali MT (2014) Flavonoid-rich beverage effects on lipid profile and blood pressure in diabetic patients. World J Diabetes 5(6):962–968. https://doi.org/10.4239/wjd.v5.i6.962

    Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Cassidy A, O’Reilly EJ, Kay C, Sampson L, Franz M, Forman JP, Curhan G, Rimm EB (2011) Habitual intake of flavonoid subclasses and incident hypertension in adults. Am J Clin Nutr 93(2):338–347. https://doi.org/10.3945/ajcn.110.006783

    CAS  Article  PubMed  Google Scholar 

  42. 42.

    Cassidy A, Mukamal KJ, Liu L, Franz M, Eliassen AH, Rimm EB (2013) High anthocyanin intake is associated with a reduced risk of myocardial infarction in young and middle-aged women. Circulation 127(2):188–196. https://doi.org/10.1161/CIRCULATIONAHA.112.122408

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Ellis CL, Edirisinghe I, Kappagoda T, Burton-Freeman B (2011) Attenuation of meal-induced inflammatory and thrombotic responses in overweight men and women after 6-week daily strawberry (Fragaria) intake. A randomized placebo-controlled trial. J Atheroscler Thromb 18(4):318–327. https://doi.org/10.5551/jat.6114

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Aranaz P, Romo-Hualde A, Zabala M, Navarro-Herrera D, Ruiz de Galarreta M, Gil AG, Martinez JA, Milagro FI, Gonzalez-Navarro CJ (2017) Freeze-dried strawberry and blueberry attenuates diet-induced obesity and insulin resistance in rats by inhibiting adipogenesis and lipogenesis. Food Funct 8(11):3999–4013. https://doi.org/10.1039/c7fo00996h

    CAS  Article  PubMed  Google Scholar 

  45. 45.

    Jiang X, Li X, Zhu C, Sun J, Tian L, Chen W, Bai W (2019) The target cells of anthocyanins in metabolic syndrome. Crit Rev Food Sci Nutr 59(6):921–946. https://doi.org/10.1080/10408398.2018.1491022

    CAS  Article  PubMed  Google Scholar 

  46. 46.

    Wu T, Yin J, Zhang G, Long H, Zheng X (2016) Mulberry and cherry anthocyanin consumption prevents oxidative stress and inflammation in diet-induced obese mice. Mol Nutr Food Res 60(3):687–694. https://doi.org/10.1002/mnfr.201500734

    CAS  Article  PubMed  Google Scholar 

  47. 47.

    Arjinajarn P, Chueakula N, Pongchaidecha A, Jaikumkao K, Chatsudthipong V, Mahatheeranont S, Norkaew O, Chattipakorn N, Lungkaphin A (2017) Anthocyanin-rich riceberry bran extract attenuates gentamicin-induced hepatotoxicity by reducing oxidative stress, inflammation and apoptosis in rats. Biomed Pharmacother 92:412–420. https://doi.org/10.1016/j.biopha.2017.05.100

    CAS  Article  PubMed  Google Scholar 

  48. 48.

    Shafie SR, Wanyonyi S, Panchal SK, Brown L (2019) Linseed components are more effective than whole linseed in reversing diet-induced metabolic syndrome in rats. Nutrients 11(7):1677. https://doi.org/10.3390/nu11071677

    CAS  Article  PubMed Central  Google Scholar 

  49. 49.

    Alvarez-Suarez JM, Giampieri F, Tulipani S, Casoli T, Di Stefano G, Gonzalez-Paramas AM, Santos-Buelga C, Busco F, Quiles JL, Cordero MD, Bompadre S, Mezzetti B, Battino M (2014) One-month strawberry-rich anthocyanin supplementation ameliorates cardiovascular risk, oxidative stress markers and platelet activation in humans. J Nutr Biochem 25(3):289–294. https://doi.org/10.1016/j.jnutbio.2013.11.002

    CAS  Article  PubMed  Google Scholar 

  50. 50.

    Prior RL, Wu X, Gu L, Hager T, Hager A, Wilkes S, Howard L (2009) Purified berry anthocyanins but not whole berries normalize lipid parameters in mice fed an obesogenic high fat diet. Mol Nutr Food Res 53(11):1406–1418. https://doi.org/10.1002/mnfr.200900026

    CAS  Article  PubMed  Google Scholar 

  51. 51.

    Jamar G, Estadella D, Pisani LP (2017) Contribution of anthocyanin-rich foods in obesity control through gut microbiota interactions. BioFactors 43(4):507–516. https://doi.org/10.1002/biof.1365

    CAS  Article  PubMed  Google Scholar 

  52. 52.

    Park E, Edirisinghe I, Wei H, Vijayakumar LP, Banaszewski K, Cappozzo JC, Burton-Freeman B (2016) A dose-response evaluation of freeze-dried strawberries independent of fiber content on metabolic indices in abdominally obese individuals with insulin resistance in a randomized, single-blinded, diet-controlled crossover trial. Mol Nutr Food Res 60(5):1099–1109. https://doi.org/10.1002/mnfr.201500845

    CAS  Article  PubMed  Google Scholar 

  53. 53.

    Paquette M, Medina Larque AS, Weisnagel SJ, Desjardins Y, Marois J, Pilon G, Dudonne S, Marette A, Jacques H (2017) Strawberry and cranberry polyphenols improve insulin sensitivity in insulin-resistant, non-diabetic adults: a parallel, double-blind, controlled and randomised clinical trial. Br J Nutr 117(4):519–531. https://doi.org/10.1017/S0007114517000393

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Miller K, Feucht W, Schmid M (2019) Bioactive compounds of strawberry and blueberry and their potential health effects based on human intervention studies: a brief overview. Nutrients 11(7):1510. https://doi.org/10.3390/nu11071510

    CAS  Article  PubMed Central  Google Scholar 

  55. 55.

    Lee YM, Yoon Y, Yoon H, Park HM, Song S, Yeum KJ (2017) Dietary anthocyanins against obesity and inflammation. Nutrients 9(10):1089. https://doi.org/10.3390/nu9101089

    CAS  Article  PubMed Central  Google Scholar 

  56. 56.

    Kim SY, Wi H-R, Choi S, Ha TJ, Lee BW, Lee M (2015) Inhibitory effect of anthocyanin-rich black soybean testa (Glycine max (L.) Merr.) on the inflammation-induced adipogenesis in a DIO mouse model. J Funct Foods 14:623–633. https://doi.org/10.1016/j.jff.2015.02.030

    CAS  Article  Google Scholar 

  57. 57.

    Yook JS, Kim KA, Kim M, Cha YS (2017) Black Adzuki bean (Vigna angularis) attenuates high-fat diet-induced colon inflammation in mice. J Med Food 20(4):367–375. https://doi.org/10.1089/jmf.2016.3821

    CAS  Article  PubMed  Google Scholar 

  58. 58.

    Wu X, Pittman HE 3rd, Prior RL (2004) Pelargonidin is absorbed and metabolized differently than cyanidin after marionberry consumption in pigs. J Nutr 134(10):2603–2610. https://doi.org/10.1093/jn/134.10.2603

    CAS  Article  PubMed  Google Scholar 

  59. 59.

    Fang J (2014) Some anthocyanins could be efficiently absorbed across the gastrointestinal mucosa: extensive presystemic metabolism reduces apparent bioavailability. J Agric Food Chem 62(18):3904–3911. https://doi.org/10.1021/jf405356b

    CAS  Article  PubMed  Google Scholar 

  60. 60.

    Warner EF, Rodriguez-Ramiro I, O’Connell MA, Kay CD (2018) Cardiovascular mechanisms of action of anthocyanins may be associated with the impact of microbial metabolites on heme oxygenase-1 in vascular smooth muscle cells. Molecules 23(4):898. https://doi.org/10.3390/molecules23040898

    CAS  Article  PubMed Central  Google Scholar 

  61. 61.

    Krga I, Tamaian R, Mercier S, Boby C, Monfoulet LE, Glibetic M, Morand C, Milenkovic D (2018) Anthocyanins and their gut metabolites attenuate monocyte adhesion and transendothelial migration through nutrigenomic mechanisms regulating endothelial cell permeability. Free Radic Biol Med 124:364–379. https://doi.org/10.1016/j.freeradbiomed.2018.06.027

    CAS  Article  PubMed  Google Scholar 

  62. 62.

    Reagan-Shaw S, Nihal M, Ahmad N (2008) Dose translation from animal to human studies revisited. FASEB J 22(3):659–661. https://doi.org/10.1096/fj.07-9574LSF

    CAS  Article  Google Scholar 

Download references

Acknowledgement

Rat urine samples were analysed for sugars at the Central Analytical Research Facility (CARF) of the Queensland University of Technology, Gardens Point, Brisbane, with the assistance of Dr. Rajesh Gupta. Gut histology was performed at the CARF, Queensland University of Technology, Kelvin Grove, Brisbane, with the assistance of Ms Felicity Lawrence. We thank Brian Bynon, School of Veterinary Sciences, The University of Queensland, Gatton, for the plasma analyses. This work was supported by funding received from the University of Southern Queensland Research and Innovation Division.

Author information

Affiliations

  1. Functional Foods Research Group, University of Southern Queensland, Toowoomba, QLD, 4350, Australia

    Naga KR Ghattamaneni, Ashwini Sharma, Sunil K. Panchal & Lindsay Brown

  2. School of Health and Wellbeing, University of Southern Queensland, Toowoomba, QLD, 4350, Australia

    Ashwini Sharma & Lindsay Brown

Authors
  1. Naga KR Ghattamaneni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ashwini Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sunil K. Panchal
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lindsay Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NKRG, SKP and LB developed the original study aims. NKRG and AS conducted the experiments. NKRG and AS analysed the data whereas NKRG, SKP and LB interpreted the data; NKRG, SKP and LB prepared manuscript drafts and contributed to the final version. LB has been the corresponding author throughout the writing process. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Lindsay Brown.

Ethics declarations

Conflicts of interest

The authors declare no conflicts of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 430 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Ghattamaneni, N.K., Sharma, A., Panchal, S.K. et al. Pelargonidin 3-glucoside-enriched strawberry attenuates symptoms of DSS-induced inflammatory bowel disease and diet-induced metabolic syndrome in rats. Eur J Nutr 59, 2905–2918 (2020). https://doi.org/10.1007/s00394-019-02130-1

Download citation

Keywords

  • Inflammatory bowel disease
  • Metabolic syndrome
  • Anthocyanin
  • Pelargonidin 3-glucoside
  • Inflammation