The synergistic effect of dietary cholesterol with fruit tannins in forming kidney stones

Abstract

Prevalence of kidney stones has increased continously over several decades worldwide, the major causes of which are largely unknown. To explore the dietary causes of kidney stones, and reveal mechanisms underlying dietary risk factors inducing kidney stones, animal experiments using mice as the disease model were performed. Eight-week old male CD-1 mice were treated by ethylene glycol, cholesterol or/and apple tannins for 3 d, respectively. In the present study, the crystalline analysis in urine and kidney tissues, HE staining kidney sections as well as observation of micro-stones, tannins and cholesterol deposition in kidneys of mice in different groups were conducted. We found that gavage with ethylene glycol, cholesterol and tannins resulted in mice urine solute supersaturation in renal tubules and forming kidney stones. Significant cholesterol and tannin deposits in mouse kidney were observed by laser confocal microscopy and crystals were shown either adhered with or co-deposited with cholesterol and tannin deposits. The primary crystals were found in renal cortex, medullar, especially papilla in the kidney sections under polarized microscope. These findings demonstrate that interaction of cholesterol and tannins in kidney plays a critical role in the formation of kidney stones.

Keywords

Polyphenol / Condensed tannins / Cholesterol / Kidney stones / Synergistic effect.

References

[1] Romero V, Akpinar H, Assimos DG. Kidney stones: a global picture of prevalence, incidence, and associated risk factors Reviews in urology. 2010, 12 2-3 e86-e96

[2] Safarinejad MR. Adult urolithiasis in a population-based study in Iran: prevalence, incidence, and associated risk factors Urological Research. 2007, 35, 73-82

[3] Sorokin I, Mamoulakis C, Miyazawa K, Rodgers A, Talati J, et al. Epidemiology of stone disease across the world World Journal of Urology. 2017, 35, 1301-20

[4] Littlejohns TJ, Neal NL, Bradbury KE, Heers H, Allen NE, et al. Fluid intake and dietary factors and the risk of incident kidney stones in UK Biobank: a population-based prospective cohort study European Urology Focus. 2020, 6 4 752-61

[5] Khalili P, Jamali Z, Sadeghi T, Esmaeili-Nadimi A, Mohamadi M, et al. Risk factors of kidney stone disease: a cross-sectional study in the southeast of Iran BMC Urology. 2021, 21, 141

[6] Huang WY, Chen YF, Carter S, Chang HC, Lan CF, et al. Epidemiology of upper urinary tract stone disease in a Taiwanese population: a nationwide, population based study The Journal of Urology. 2013, 189 6 2158-63

[7] Trinchieri A. Epidemiological trends in urolithiasis: impact on our health care systems Urological Research. 2006, 34, 151-56

[8] Kirkali Z, Rasooly R, Star RA, Rodgers GP. Urinary stone disease: progress, status, and needs Urology. 2015, 86 4 651-53

[9] Worcester EM, Coe FL. Nephrolithiasis Primary Care: Clinics in Office Practice. 2008, 35 2 369-91

[10] Friedlander JI, Antonelli JA, Pearle MS. Diet: from food to stone World Journal of Urology. 2015, 33, 179-85

[11] Siener R. Impact of dietary habits on stone incidence Urological Research. 2006, 34, 131-33

[12] Konjengbam H, Meitei SY. Association of kidney stone disease with dietary factors: a review Anthropological Review. 2020, 83 1 65-73

[13] Chewcharat A, Thongprayoon C, Vaughan LE, Mehta RA, Schulte PJ, et al. Dietary risk factors for incident and recurrent symptomatic kidney stones Mayo Clinic Proceedings. 2022, 97 8 1437-48

[14] Curhan GC, Willett WC, Speizer FE, Spiegelman D, Stampfer MJ. Comparison of dietary calcium with supplemental calcium and other nutrients as factors affecting the risk for kidney stones in women Annals of Internal Medicine. 1997, 126, 497-504

[15] Holmes RP, Goodman HO, Assimos DG. Contribution of dietary oxalate to urinary oxalate excretion Kidney International. 2001, 59 1 270-76

[16] Borghi L, Meschi T, Maggiore U, Prati B. Dietary therapy in idiopathic nephrolithiasis Nutrition Reviews. 2006, 64 7 301-12

[17] Coe FL, Evan AP, Worcester EM, Lingeman JE. Three pathways for human kidney stone formation Urological Research. 2010, 38, 147-60

[18] He FJ, Nowson CA, MacGregor GA. Fruit and vegetable consumption and stroke: meta-analysis of cohort studies The Lancet. 2006, 367 9507 320-26

[19] Portincasa P, Moschetta A, Palasciano G. Cholesterol gallstone disease The Lancet. 2006, 368 9531 230-39

[20] Xi Y, Cheng D, Zeng X, Cao J, Jiang W. Evidences for chlorogenic acid — a major endogenous polyphenol involved in regulation of ripening and senescence of apple fruit PLoS One. 2016, 11, e0146940

[21] Okada A, Nomura S, Higashibata Y, Hirose M, Gao B, et al. Successful formation of calcium oxalate crystal deposition in mouse kidney by intraabdominal glyoxylate injection Urological Research. 2007, 35, 89-99

[22] Paragas N, Qiu A, Zhang Q, Samstein B, Deng SX, et al. The Ngal reporter mouse detects the response of the kidney to injury in real time Nature Medicine. 2011, 17 2 216-22

[23] Agapova OA, Fang Y, Sugatani T, Seifert ME, Hruska KA. Ligand trap for the activin type IIA receptor protects against vascular disease and renal fibrosis in mice with chronic kidney disease Kidney International. 2016, 89 6 1231-43

[24] Schepers MS, Duim RA, Asselman M, Romijn JC, Schröder FH, et al. Internalization of calcium oxalate crystals by renal tubular cells: a nephron segment-specific process? Kidney International. 2003, 64 2 493-500

[25] Ioannou GN, Van Rooyen DM, Savard C, Haigh WG, Yeh MM, et al. Cholesterol-lowering drugs cause dissolution of cholesterol crystals and disperse Kupffer cell crown-like structures during resolution of NASH Journal of Lipid Research. 2015, 56 2 277-85

[26] De SK, Liu X, Monga M. Changing trends in the American diet and the rising prevalence of kidney stones Urology. 2014, 84 5 1030-33

[27] Fink HA, Akornor JW, Garimella PS, MacDonald R, Cutting A, et al. Diet, fluid, or supplements for secondary prevention of nephrolithiasis: a systematic review and meta-analysis of randomized trials European Urology. 2009, 56 1 72-80

[28] Guan N, Fan Q, Ding J, Zhao Y, Lu J, et al. Melamine-contaminated powdered formula and urolithiasis in young children New England Journal of Medicine. 2009, 360 1 1067-74

[29] Ferraro PM, Bargagli M, Trinchieri A, Gambaro G. Risk of kidney stones: influence of dietary factors, dietary patterns, and vegetarian–vegan diets Nutrients. 2020, 12 3 779

[30] Jackson RD, LaCroix AZ, Gass M, Wallace RB, Robbins J, et al. Calcium plus vitamin D supplementation and the risk of fractures New England Journal of Medicine. 2006, 354 7 669-83

[31] Taylor EN, Stampfer MJ, Curhan GC. Obesity, weight gain, and the risk of kidney stones JAMA. 2005, 293 4 455-62

[32] Miettinen TA, Gylling H. Cholesterol absorption efficiency and sterol metabolism in obesity Atherosclerosis. 2000, 153 1 241-48

[33] Hagerman AE, Riedl KM, Jones GA, Sovik KN, Ritchard NT, et al. High molecular weight plant polyphenolics (tannins) as biological antioxidants Journal of Agricultural and Food Chemistry. 1998, 46 5 1887-92

[34] Baker PW, Coyle P, Bais R, Rofe AM. Influence of season, age, and sex on renal stone formation in South Australia Medical journal of Australia. 1993, 159 6 390-92

[35] Sorensen MD, Hsi RS, Chi T, Shara N, Wactawski-Wende J, et al. Dietary intake of fiber, fruit and vegetables decreases the risk of incident kidney stones in women: a women’s health initiative report The Journal of Urology. 2014, 192 6 1694-99

[36] Schmiedl A, Schwille PO, Bonucci E, Erben RG, Grayczyk A, et al. Nephrocalcinosis and hyperlipidemia in rats fed a cholesterol- and fat-rich diet: association with hyperoxaluria, altered kidney and bone minerals, and renal tissue phospholipid–calcium interaction Urological Research. 2000, 28 6 404-15

This work was supported by the National Natural Science Foundation of China (No.32172270).

RIGHTS & PERMISSIONS

2023 Editorial Office of Food Innovation and Advances