Abstract
Cranberry juice is increasingly consumed for its richness in polyphenols having a positive impact on human health. Unfortunately, when regularly consumed, its high concentration in organic acids may cause some intestinal discomforts. In the present study, its organic acid content was reduced of 41% by electrodialysis with bipolar membrane (EDBM), and the resulted deacidified juice was divided in five different juices readjusted or not with different concentrations of citric and/or malic acid(s) corresponding to the concentration of this/these acid(s) recovered during EDBM or at the titratable acidity (TA) of the non-deacidified cranberry juice. The evolution of the cranberry juice main interesting compounds (organic acids and polyphenols), according to the concentration and nature of the organic acids present, was studied for the first time at each specific stages of the digestion. After digestion, Caco-2 cells were exposed to all digested juices to identify the organic acid(s) responsible for the loss of integrity of the epithelial barrier. It appeared that organic acid contents did not change during the different steps of the digestion while polyphenolic compounds decreased starting from the gastric phase. Whatever the organic acid concentration or nature, the concentration of PACs significantly decreased between the salivary and the gastric steps but was different according to their structure when the concentration of most of anthocyanins significantly decreased at the gastric step. Also, to the best of our knowledge, it was the first time that citric acid was demonstrated as the organic acid responsible for the loss of integrity of Caco-2 cell monolayers.
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References
Bazinet L, Ippersiel D, Mahdavi B (2004) Fractionation of whey proteins by bipolar membrane electroacidification. Innov Food Sci Emerg Technol 5:17–25. https://doi.org/10.1016/j.ifset.2003.10.001
Bazinet L, Brianceau S, Dubé P, Desjardins Y (2012) Evolution of cranberry juice physico-chemical parameters during phenolic antioxidant enrichment by electrodialysis with filtration membrane. Sep Purif Technol 87:31–39. https://doi.org/10.1016/j.seppur.2011.11.017
Bermúdez-Soto M-J, Tomás-Barberán F-A, García-Conesa M-T (2007) Stability of polyphenols in chokeberry (Aronia melanocarpa) subjected to in vitro gastric and pancreatic digestion. Food Chem 102:865–874. https://doi.org/10.1016/j.foodchem.2006.06.025
Cho MJ, Scieszka JF, Burton PS (1989) Citric acid as an adjuvant for transepithelial transport. Int J Pharm 52:79–81. https://doi.org/10.1016/0378-5173(89)90091-4
Daugherty AL, Mrsny RJ (1999) Regulation of the intestinal epithelial paracellular barrier. Pharm Sci Technol Today 2:281–287. https://doi.org/10.1016/S1461-5347(99)00170-4
Déprez S, Brezillon C, Rabot S, Philippe C, Mila I, Lapierre C, Scalbert A (2000) Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids. J Nutr 130:2733–2738. https://doi.org/10.1093/jn/130.11.2733
Faucher M, Serre É, Langevin M-È, Mikhaylin S, Lutin F, Bazinet L (2018) Drastic energy consumption reduction and ecoefficiency improvement of cranberry juice deacidification by electrodialysis with bipolar membranes at semi-industrial scale: reuse of the recovery solution. J Membr Sci 555:105–114. https://doi.org/10.1016/j.memsci.2018.02.041
Froment DPH, Molitoris BA, Buddington B, Miller N, Alfrey AC (1989) Site and mechanism of enhanced gastrointestinal absorption of aluminum by citrate. Kidney Int 36:978–984. https://doi.org/10.1038/ki.1989.290
Gupta A, Bansal K, Marwaha M (2015) Effect of high-molecular-weight component of Cranberry on plaque and salivary Streptococcus mutans counts in children: an in vivo study. J Indian Soc Pedod Prev Dent 33(2):128. https://doi.org/10.4103/0970-4388.155125
Hayashi M, Sakai T, Hasegawa Y, Nishikawahara T, Tomioka H, Iida A, Shimizu N, Tomita M, Awazu S (1999) Physiological mechanism for enhancement of paracellular drug transport. J Control Release 62:141–148. https://doi.org/10.1016/S0168-3659(99)00031-0
He J, Wallace TC, Keatley KE, Failla ML, Giusti MM (2009) Stability of black raspberry anthocyanins in the digestive tract lumen and transport efficiency into gastric and small intestinal tissues in the rat. J Agric Food Chem 57:3141–3148. https://doi.org/10.1021/jf900567t
Hidalgo IJ, Raub TJ, Borchardt RT (1989) Characterization of the human colon carcinoma cell line (Caco-2) as a model system for intestinal epithelial permeability. Gastroenterology 96:736–749. https://doi.org/10.1016/S0016-5085(89)80072-1
Kamonpatana K, Giusti MM, Chitchumroonchokchai C, MorenoCruz M, Riedl KM, Kumar P, Failla ML (2012) Susceptibility of anthocyanins to ex vivo degradation in human saliva. Food Chem 135:738–747. https://doi.org/10.1016/j.foodchem.2012.04.110
Khanal RC, Howard LR, Brownmiller CR, Prior RL (2009) Influence of extrusion processing on procyanidin composition and total anthocyanin contents of blueberry pomace. J Food Sci 74:H52–H58. https://doi.org/10.1111/j.1750-3841.2009.01063.x
Mani KN (1991) Electrodialysis water splitting technology. J Membr Sci 58:117–138. https://doi.org/10.1016/S0376-7388(00)82450-3
MAPAQ (2018) Portrait diagnostique-sectoriel de la canneberge au Québec
Março PH, Scarminio IS (2007) Q-mode curve resolution of UV–vis spectra for structural transformation studies of anthocyanins in acidic solutions. Anal Chim Acta 583:138–146. https://doi.org/10.1016/j.aca.2006.09.057
McKay DL, Blumberg JB (2007) Cranberries (Vaccinium macrocarpon) and cardiovascular disease risk factors. Nutr Rev 65:490–502
Mosele JI, Macià A, Romero M-P, Motilva M-J, Rubió L (2015) Application of in vitro gastrointestinal digestion and colonic fermentation models to pomegranate products (juice, pulp and peel extract) to study the stability and catabolism of phenolic compounds. J Funct Foods 14:529–540. https://doi.org/10.1016/j.jff.2015.02.026
Noach ABJ, Kurosaki Y, Blom-Roosemalen MCM, de Boer AG, Breimer DD (1993) Cell-polarity dependent effect of chelation on the paracellular permeability of confluent caco-2 cell monolayers. Int J Pharm 90:229–237. https://doi.org/10.1016/0378-5173(93)90195-L
Nolan CR, Califano JR, Butzin CA (1990) Influence of calcium acetate or calcium citrate on intestinal aluminum absorption. Kidney Int 38:937–941. https://doi.org/10.1038/ki.1990.294
Sartor RB (2006) Mechanisms of disease: pathogenesis of Crohn’s disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 3:390–407. https://doi.org/10.1038/ncpgasthep0528
Serre E, Boutin Y, Langevin M-E, Lutin F, Pedneault K, Lacour S, Bazinet L (2016a) Deacidification of cranberry juice protects against disruption of in vitro intestinal cell barrier integrity. J Funct Foods 26:208–216. https://doi.org/10.1016/j.jff.2016.06.021
Serre E, Rozoy E, Pedneault K, Lacour S, Bazinet L (2016b) Deacidification of cranberry juice by electrodialysis: impact of membrane types and configurations on acid migration and juice physicochemical characteristics. Sep Purif Technol 163:228–237. https://doi.org/10.1016/j.seppur.2016.02.044
Spencer JPE, Chaudry F, Pannala AS, Srai SK, Debnam E, Rice-Evans C (2000) Decomposition of cocoa procyanidins in the gastric milieu. Biochem Biophys Res Commun 272:236–241. https://doi.org/10.1006/bbrc.2000.2749
Srinivasan B, Kolli AR, Esch MB, Abaci HE, Shuler ML, Hickman JJ (2015) TEER measurement techniques for in vitro barrier model systems. J Lab Autom 20:107–126. https://doi.org/10.1177/2211068214561025
Sun J, Marais JPJ, Khoo C, LaPlante K, Vejborg RM, Givskov M, Tolker-Nielsen T, Seeram NP, Rowley DC (2015) Cranberry (Vaccinium macrocarpon) oligosaccharides decrease biofilm formation by uropathogenic Escherichia coli. J Funct Foods 17:235–242. https://doi.org/10.1016/j.jff.2015.05.016
Tomita M, Hayashi M, Awazu S (1996) Absorption-enhancing mechanism of EDTA, caprate, and decanoylcarnitine in Caco-2 cells. J Pharm Sci 85:608–611. https://doi.org/10.1021/js9504604
Vasileiou I, Katsargyris A, Theocharis S, Giaginis C (2013) Current clinical status on the preventive effects of cranberry consumption against urinary tract infections. Nutr Res 33:595–607. https://doi.org/10.1016/j.nutres.2013.05.018
Versantvoort CHM, Oomen AG, Van de Kamp E, Rompelberg CJM, Sips AJAM (2005) Applicability of an in vitro digestion model in assessing the bioaccessibility of mycotoxins from food. Food Chem Toxicol 43:31–40. https://doi.org/10.1016/j.fct.2004.08.007
Wada L, Ou B (2002) Antioxidant activity and phenolic content of Oregon caneberries. J Agric Food Chem 50:3495–3500. https://doi.org/10.1021/jf011405l
Weerachayaphorn J, Pajor AM (2008) Identification of transport pathways for citric acid cycle intermediates in the human colon carcinoma cell line, Caco-2. Biochim Biophys Acta BBA Biomembr 1778:1051–1059. https://doi.org/10.1016/j.bbamem.2007.12.013
Wing DA, Rumney PJ, Preslicka CW, Chung JH (2008) Daily cranberry juice for the prevention of asymptomatic bacteriuria in pregnancy: a randomized, controlled pilot study. J Urol 180:1367–1372
Wu X, Prior RL (2005) Systematic identification and characterization of anthocyanins by HPLC-ESI-MS/MS in common foods in the United States: fruits and berries. J Agric Food Chem 53:2589–2599. https://doi.org/10.1021/jf048068b
Yang P, Yuan C, Wang H, Han F, Liu Yangjie, Wang L, Liu Yang (2018) Stability of anthocyanins and their degradation products from cabernet sauvignon red wine under gastrointestinal ph and temperature conditions. Molecules 23:354. https://doi.org/10.3390/molecules23020354
Zhao L, Temelli F (2017) Preparation of anthocyanin-loaded liposomes using an improved supercritical carbon dioxide method. Innov Food Sci Emerg Technol 39:119–128. https://doi.org/10.1016/j.ifset.2016.11.013
Acknowledgements
The financial support of the Natural Sciences and Engineering Research Council of Canada (NSERC) is acknowledged. This work was supported by the NSERC Industrial Research Chair on Electromembrane processes aiming the ecoefficiency improvement of biofood production lines (Grant IRCPJ 492889-15 to Laurent Bazinet). The authors thank Mrs. Véronique Richard (Institute of Nutrition and Functional Foods (INAF)) for technical assistance with HPLC analysis.
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Renaud, V., Faucher, M., Perreault, V. et al. Evolution of cranberry juice compounds during in vitro digestion and identification of the organic acid responsible for the disruption of in vitro intestinal cell barrier integrity. J Food Sci Technol 57, 2329–2342 (2020). https://doi.org/10.1007/s13197-020-04271-2
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DOI: https://doi.org/10.1007/s13197-020-04271-2