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Research Article

Differences in P-Type and Type 1 Uropathogenic Escherichia coli Urinary Anti-Adhesion Activity of Cranberry Fruit Juice Dry Extract Product and D-Mannose Dietary Supplement

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References

  • Ala-Jaakkola R, Laitila A, Ouwehand AC, Lehtoranta L. 2022. Role of D-mannose in urinary tract infections - a narrative review. Nutr J. 21(1):18. doi: 10.1186/s12937-022-00769-x.
  • Beachey EH. 1981. Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. J Infect Dis. 143(3):325–345. doi: 10.1093/infdis/143.3.325.
  • Bekiares N, Krueger CG, Meudt JJ, Shanmuganayagam D, Reed JD. 2018. Effect of sweetened dried cranberry consumption on urinary proteome and fecal microbiome in healthy human subjects. OMICS. 22(2):145–153. doi: 10.1089/omi.2016.0167.
  • Birmingham AD, Esquivel-Alvarado D, Maranan M, Krueger CG, Reed JD. 2021. Inter-laboratory validation of 4-(dimethylamino) cinnamaldehyde (DMAC) assay using cranberry proanthocyanidin standard for quantification of soluble proanthocyanidins in cranberry foods and dietary supplements, First action official method SM: 2019.06. J AOAC Int. 104(1):216–222. doi: 10.1093/jaoacint/qsaa084.
  • Bosley S, Krueger CG, Birmingham A, Howell AB, Reed JD. 2024. Improved in vitro hemagglutination assays utilizing P-Type and Type 1 uropathogenic Escherichia coli to evaluate bacterial anti-adhesion activity of cranberry products. J Diet Suppl. 21(3):327–343. doi: 10.1080/19390211.2023.2276962.
  • Chughtai B, Thomas D, Howell A. 2016. Variability of commercial cranberry dietary supplements for the prevention of uropathogenic bacterial adhesion. Am J Obstet Gynecol. 215(1):122–123. doi: 10.1016/j.ajog.2016.03.046.
  • Cooper TE, Teng C, Howell M, Teixeira-Pinto A, Jaure A, Wong G. 2022. D-mannose for preventing and treating urinary tract infections. Cochrane Database Syst Rev. 8(8):CD013608. doi: 10.1002/14651858.CD013608.pub2.
  • Cunningham DG, Vannozzi S, O’Shea E, Turk R. 2002. Analysis and standardization of cranberry products. In: Ho CT, Zheng QY, editors. Quality management of nutraceuticals. Washington (DC): American Chemical Society; p. 151–166.
  • DE Leo V, Cappelli V, Massaro MG, Tosti C, Morgante G. 2017. Evaluation of the effects of a natural dietary supplement with cranberry, Noxamicina® and D-mannose in recurrent urinary infections in perimenopausal women. Minerva Ginecol. 69(4):336–341. doi: 10.23736/S0026-4784.17.04074-6.
  • de Llano DG, Esteban-Fernández A, Sánchez-Patán F, Martínlvarez PJ, Moreno-Arribas MV, Bartolomé B. 2015. Anti-adhesive activity of cranberry phenolic compounds and their microbial-derived metabolites against uropathogenic Escherichia coli in bladder epithelial cell cultures. Int J Mol Sci. 16(6):12119–12130.
  • Del Popolo G, Nelli F. 2018. Recurrent bacterial symptomatic cystitis: a pilot study on a new natural option for treatment. Arch Ital Urol Androl. 90(2):101–103. doi: 10.4081/aiua.2018.2.101.
  • Déprez S, Brezillo C, Rabot S, Philippe C, Mila I, Lapierre C, et al. 2000. Polymeric proanthocyanidins are catabolized by human colonic microflora into low-molecular-weight phenolic acids. J. Nutr. 130:2733–2738.
  • Di Martino P, Agniel R, David K, Templer C, Gaillard JL, Denys P, Botto H. 2006. Reduction of Escherichia coli adherence to uroepithelial bladder cells after consumption of cranberry juice: a double-blind randomized placebo-controlled cross-over trial. World J Urol. 24(1):21–27. doi: 10.1007/s00345-005-0045-z.
  • Diaz MS, Mertens-Talcott SU, Talcott ST. 2024. Intestinal microbiome metabolism of cranberry (Vaccinium macrocarpon) proanthocyanidin dimers, but not trimers, is altered by dysbiosis in ulcerative colitis ex vivo. J Agric Food Chem. 72(8):4184–4194. doi: 10.1021/acs.jafc.4c00042.
  • Esquivel-Alvarado D, Alfaro-Viquez E, Krueger CG, Vestling MM, Reed JD. 2021. Identification of A-type proanthocyanidins in cranberry-based foods and dietary supplements by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry, First Action Method: 2019.05. J AOAC Int. 104(1):223–231. doi: 10.1093/jaoacint/qsaa106.
  • Fan E, Dashti M, Fuentes J, Reitzer L, Christie AL, Zimmern PE. 2023. D-mannosuria levels measured 1 h after d-mannose intake can select out favorable responders: A pilot study. Neurourol Urodyn. 42(1):49–55. doi: 10.1002/nau.25059.
  • Feldman M, Weiss EI, Ofek I, Steinberg D. 2009. Interference of cranberry constituents in cell-cell signaling system of Vibrio harveyi. Curr Microbiol. 59(4):469–474. doi: 10.1007/s00284-009-9462-3.
  • Feliciano RP, Boeres A, Massacessi L, Istas G, Ventura MR, Nunes Dos Santos C, Heiss C, Rodriguez-Mateos A. 2016. Identification and quantification of novel cranberry-derived plasma and urinary (poly)phenols. Arch Biochem Biophys. 599:31–41. doi: 10.1016/j.abb.2016.01.014.
  • Feliciano RP, Mills CE, Istas G, Heiss C, Rodriguez-Mateos A. 2017. Absorption, metabolism and excretion of cranberry (poly)phenols in humans: a dose response study and assessment of inter-individual variability. Nutrients. 9(3):268. doi: 10.3390/nu9030268.
  • Foo LY, Lu Y, Howell AB, Vorsa N. 2000a. The structure of cranberry proanthocyanidins which inhibit adherence of uropathogenic P-fimbriated Escherichia coli in vitro. Phytochemistry. 54(2):173–181. doi: 10.1016/S0031-9422(99)00573-7.
  • Foo LY, Lu Y, Howell AB, Vorsa N. 2000b. A-type proanthocyanidin trimers from cranberry that inhibit adherence of uropathogenic P-fimbriated Escherichia coli. J Nat Prod. 63(9):1225–1228. doi: 10.1021/np000128u.
  • Gazi U, Martinez-Pomares L. 2009. Influence of the mannose receptor in host immune responses. Immunobiology. 214(7):554–561. doi: 10.1016/j.imbio.2008.11.004.
  • Global antimicrobial resistance and use surveillance system (GLASS) report 2022. 2022. Geneva: World Health Organization.
  • Gullickson ER, Krueger CG, Birmingham A, Maranan M, Reed JD. 2020. Development of a cranberry standard for quantification of insoluble cranberry (Vaccinium macrocarpon Ait.) proanthocyanidins. J Agric Food Chem. 68(10):2900–2905. doi: 10.1021/acs.jafc.9b03696.
  • Gupta K, Chou MY, Howell A, Wobbe C, Grady R, Stapleton AE. 2007. Cranberry products inhibit adherence of uropathogenic Escherichia coli to primary cultured bladder and vaginal epithelial cells. J Urol. 177(6):2357–2360. doi: 10.1016/j.juro.2007.01.114.
  • Hagberg L, Jodal U, Korhonen T, Lidin-Janson G, Lindberg U, Svanborg E. 1981. Adhesion, hemagglutination, and virulence of Escherichia coli causing urinary tract infections. Infect Immun. 31(2):564–570. doi: 10.1128/iai.31.2.564-570.1981.
  • Hotchkiss AT, Jr., Nunez A, Strahan GD, Chau HK, White AK, Marais JP, et al. 2015. Cranberry xyloglucan structure and inhibition of Escherichia coli adhesion to epithelial cells. J Agric Food Chem. 63(23):5622–5633. doi: 10.1021/acs.jafc.5b00730.
  • Howell A, Souza D, Roller M, Fromentin E. 2015. Comparison of the anti-adhesion activity of three different cranberry extracts on uropathogenic P-fimbriated Escherichia coli: a randomized, double-blind, placebo controlled, ex vivo, acute study. Nat Prod Commun. 10(7):1215–1218.
  • Howell AB, Botto H, Combescure C, Blanc-Potard A-B, Gausa L, Matsumoto T, Tenke P, Sotto A, Lavigne J-P. 2010. Dosage effect on uropathogenic Escherichia coli anti-adhesion activity in urine following consumption of cranberry powder standardized for proanthocyanidin content: a multicentric randomized double blind study. BMC Infect Dis. 10(1):94. doi: 10.1186/1471-2334-10-94.
  • Howell AB, Dreyfus JF, Chughtai B. 2022. Differences in urinary bacterial anti-adhesion activity after intake of cranberry dietary supplements with soluble versus insoluble proanthocyanidins. J Diet Suppl. 19(5):621–639. doi: 10.1080/19390211.2021.1908480.
  • Howell AB, Reed JD, Krueger CG, Winterbottom R, Cunningham DG, Leahy M. 2005. A-type cranberry proanthocyanidins and uropathogenic bacterial anti-adhesion activity. Phytochemistry. 66(18):2281–2291. doi: 10.1016/j.phytochem.2005.05.022.
  • Howell AB, Vorsa N, Der Marderosian A, Foo LY. 1998. Inhibition of the adherence of P fimbriated Escherichia coli to uroepithelial-cell surfaces by proanthocyanidin extracts from cranberries. N Engl J Med. 339(15):1085–1086. doi: 10.1056/NEJM199810083391516.
  • Hu X, Shi Y, Zhang P, Miao M, Zhang T, Jiang B. 2016. D-Mannose: properties, production, and applications: an overview. Compr Rev Food Sci Food Saf. 15(4):773–785.
  • Jepson RG, Williams G, Craig JC. 2012. Cranberries for preventing urinary tract infections. Cochrane Database Syst Rev. 10(10):CD001321.
  • Johnson JR, Brown JJ, Ahmed P. 1998. Diversity of hemagglutination phenotypes among P-fimbriated wild-type strains of Escherichia coli in relation to papG allele repertoire. Clin Diagn Lab Immunol. 5(2):160–170. doi: 10.1128/CDLI.5.2.160-170.1998.
  • Johnson-White B, Buquo L, Zeinali M, Ligler FS. 2006. Prevention of nonspecific bacterial cell adhesion in immunoassays by use of cranberry juice. Anal Chem. 78(3):853–857. doi: 10.1021/ac051700v.
  • Kaspar KL, Howell AB, Khoo C. 2015. A randomized, double-blind, placebo-controlled trial to assess the bacterial anti-adhesion effects of cranberry extract beverages. Food Funct. 6(4):1212–1217. doi: 10.1039/C4FO01018C.
  • Klinth JE, Pinkner JS, Hultgren SJ, Almqvist F, Uhlin BE, Axner O. 2012. Impairment of the biomechanical compliance of P pili: a novel means of inhibiting uropathogenic bacterial infections? Eur Biophys J. 41(3):285–295. doi: 10.1007/s00249-011-0784-2.
  • Kranjčec B, Papeš D, Altarac S. 2014. D-Mannose powder for prophylaxis of recurrent urinary tract infections in women: a randomized clinical trial. World J Urol. 32(1):79–84. doi: 10.1007/s00345-013-1091-6.
  • Krueger CG, Reed JD, Feliciano RP, Howell AB. 2013. Quantifying and characterizing proanthocyanidins in cranberries in relation to urinary tract health. Anal Bioanal Chem. 405(13):4385–4395. doi: 10.1007/s00216-013-6750-3.
  • Kyriakides R, Jones P, Somani BK. 2021. Role of D-mannose in the prevention of recurrent urinary tract infections: evidence from a systematic review of the literature. Eur Urol Focus. 7(5):1166–1169. doi: 10.1016/j.euf.2020.09.004.
  • LaFavers KA, Micanovic R, Sabo AR, Maghak LA, El-Achkar TM. 2022. Evolving concepts in uromodulin biology, physiology, and its role in disease: a tale of two forms. Hypertension. 79(11):2409–2418. doi: 10.1161/hypertensionaha.122.18567.
  • Lavigne JP, Bourg G, Combescure C, Botto H, Sotto A. 2008. In-vitro and in-vivo evidence of dose-dependent decrease of uropathogenic Escherichia coli virulence after consumption of commercial Vaccinium macrocarpon (cranberry) capsules. Clin Microbiol Infect. 14(4):350–355.
  • Lee SJ, Evers S, Roeder D, Parlow AF, Risteli J, Risteli L, Lee YC, Feizi T, Langen H, Nussenzweig MC, et al. 2002. Mannose receptor-mediated regulation of serum glycoprotein homeostasis. Science. 295(5561):1898–1901. doi: 10.1126/science.1069540.
  • Lessard-Lord J, Roussel C, Guay V, Desjardins Y. 2024. Assessing the gut microbiota’s ability to metabolize oligomeric and polymeric flavan-3-ols from aronia and cranberry. Mol Nutr Food Res. 68(5):e2300641. doi: 10.1002/mnfr.202300641.
  • Liu H, Howell AB, Zhang DJ, Khoo C. 2019. A randomized, double-blind, placebo-controlled pilot study to assess bacterial anti-adhesive activity in human urine following consumption of a cranberry supplement. Food Funct. 10(12):7645–7652. doi: 10.1039/C9FO01198F.
  • Mannino G, Di Stefano V, Lauria A, Pitonzo R, Gentile C. 2020. Vaccinium macrocarpon (cranberry)-based dietary supplements: variation in mass uniformity, proanthocyanidin dosage and anthocyanin profile demonstrates quality control standard needed. Nutrients. 12(4):992. doi: 10.3390/nu12040992.
  • Melican K, Sandoval RM, Kader A, Josefsson L, Tanner GA, Molitoris BA, Richter-Dahlfors A. 2011. Uropathogenic Escherichia coli P and Type 1 fimbriae act in synergy in a living host to facilitate renal colonization leading to nephron obstruction. PLoS Pathog. 7(2):e1001298. doi: 10.1371/journal.ppat.1001298.
  • Mena P, Calani L, Bruni R, Del Rio D. 2015. Chapter 6 - Bioactivation of high-molecular-weight polyphenols by the gut microbiome. In: Kieran T, Del Rio D, editors. Diet-microbe interactions in the gut. Academic Press, London; p. 73–101. ISBN 9780124078253, doi: 10.1016/B978-0-12-407825-3.
  • Monagas M, Urpi-Sarda M, Sánchez-Patán F, Llorach R, Garrido I, Gómez-Cordovés C, Andres-Lacueva C, Bartolomé B. 2010. Insights into the metabolism and microbial biotransformation of dietary flavan-3-ols and the bioactivity of their metabolites. Food Funct. 1(3):233–253. doi: 10.1039/c0fo00132e.
  • Monagas M. 2023. Cranberry fruit juice dry extract, USP Monograph. Pharmacopeial Forum. 48(3):1–4. doi: 10.31003/USPNF_M8506_02_01.
  • Mulvey MA. 2002. Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol. 4(5):257–271. doi: 10.1046/j.1462-5822.2002.00193.x.
  • Mydock-McGrane L, Cusumano Z, Han Z, Binkley J, Kostakioti M, Hannan T, et al. 2016. Antivirulence c-mannosides as antibiotic-sparing, oral therapeutics for urinary tract infections. J Med Chem. 59(20):9390–9408.
  • Nemzer BV, Al-Taher F, Yashin A, Revelsky I, Yashin Y. 2022. Cranberry: chemical composition, antioxidant activity and impact on human health: overview. Molecules. 27(5):1503. doi: 10.3390/molecules27051503.
  • Ofek I, Hasty DL, Sharon N. 2003. Anti-adhesion therapy of bacterial diseases: prospects and problems. FEMS Immunol Med Microbiol. 38(3):181–191. doi: 10.1016/S0928-8244(03)00228-1.
  • Olden M, Corre T, Hayward C, Toniolo D, Ulivi S, Gasparini P, Pistis G, Hwang S-J, Bergmann S, Campbell H, et al. 2014. Common variants in UMOD associate with urinary uromodulin levels: a meta-analysis. J Am Soc Nephrol. 25(8):1869–1882. doi: 10.1681/ASN.2013070781.
  • Pitkänen E. 1996. Mannose, mannitol, fructose and 1,5-anhydroglucitol concentrations measured by gas chromatography/mass spectrometry in blood plasma of diabetic patients. Clin Chim Acta. 251(1):91–103. doi: 10.1016/0009-8981(96)06284-5.
  • Pruijm M, Ponte B, Ackermann D, Paccaud F, Guessous I, Ehret G, Pechère-Bertschi A, Vogt B, Mohaupt MG, Martin P-Y, et al. 2016. Associations of urinary uromodulin with clinical characteristics and markers of tubular function in the general population. Clin J Am Soc Nephrol. 11(1):70–80. doi: 10.2215/CJN.04230415.
  • Rafsanjany N, Senker J, Brandt S, Dobrindt U, Hensel A. 2015. In vivo consumption of cranberry exerts ex vivo antiadhesive activity against fimh-dominated uropathogenic Escherichia coli: a combined in vivo, ex vivo, and in vitro study of an extract from Vaccinium macrocarpon. J Agric Food Chem. 63(40):8804–8818. doi: 10.1021/acs.jafc.5b03030.
  • Reinhart H, Obedeanu N, Hooton T, Stamm W, Sobel J. 1990. Urinary excretion of Tamm-Horsfall protein in women with recurrent urinary tract infections. J Urol. 144(5):1185–1187. doi: 10.1016/s00225347(17)39687-8.
  • Roopchand DE, Krueger CG, Moskal K, Fridlender B, Lila MA, Raskin I. 2013. Food-compatible method for the efficient extraction and stabilization of cranberry pomace polyphenols. Food Chem. 141(4):3664–3669. doi: 10.1016/j.foodchem.2013.06.050.
  • Russo E, Montt Guevara M, Giannini A, Mannella P, Palla G, Caretto M, Pancetti F, Genazzani AD, Simoncini T. 2020. Cranberry, D-mannose and anti-inflammatory agents prevent lower urinary tract symptoms in women undergoing prolapse surgery. Climacteric. 23(2):201–205. doi: 10.1080/13697137.2019.1679110.
  • Säemann MD, Weichhart T, Hörl WH, Zlabinger GJ. 2005. Tamm-Horsfall protein: a multilayered defense molecule against urinary tract infection. Eur J Clin Invest. 35(4):227–235. doi: 10.1111/j.13652362.2005.01483.x.
  • Scaglione F, Minghetti P, Ambrosio F, Ernst B, Ficarra V, Gobbi M, Naber K, Schellekens H. 2023. Nature of the interaction of alpha-d-mannose and Escherichia coli bacteria, and implications for its regulatory classification. a Delphi Panel European consensus based on chemistry and legal evidence. Ther Innov Regul Sci. 57(6):1153–1166. doi: 10.1007/s43441-023-00548-8.
  • Scharenberg M, Schwardt O, Rabbani S, Ernst B. 2012. Target selectivity of fimh antagonists. J Med Chem. 55(22):9810–9816. doi: 10.1021/jm3010338.
  • Scharf B, Schmidt TJ, Rabbani S, Stork C, Dobrindt U, Sendker J, Ernst B, Hensel A. 2020. Antiadhesive natural products against uropathogenic E. coli: what can we learn from cranberry extract? J Ethnopharmacol. 257:112889. doi: 10.1016/j.jep.2020.112889.
  • Scharf B, Sendker J, Dobrindt U, Hensel A. 2019. Influence of cranberry extract on Tamm-Horsfall protein in human urine and its antiadhesive activity against uropathogenic Escherichia coli. Planta Med. 85(2):126–138. doi: 10.1055/a-0755-7801.
  • Sintara M, Li L, Cunningham DG, Prior RL, Wu X, Chang T. 2018. Single-laboratory validation for determination of total soluble proanthocyanidins in cranberry using 4 dimethylaminocinnamaldehyde. J AOAC Int. 101(3):805–809. doi: 10.5740/jaoacint.17-0288.
  • Sintara M, Wang Y, Li L, Liu H, Cunningham DG, Prior RR, Chen P, Chang T, Wu X. 2020. Quantification of cranberry proanthocyanidins by normal-phase high-performance liquid chromatography using relative response factors. Phytochem Anal. 31(6):874–883. doi: 10.1002/pca.2952.
  • Sobota AE. 1984. Inhibition of bacterial adherence by cranberry juice: potential use for the treatment of urinary tract infections. J Urol. 131(5):1013–1016. doi: 10.1016/S0022-5347(17)50751-X.
  • Spaulding CN, Klein RD, Ruer S, Kau AL, Schreiber HL, Cusumano ZT, Dodson KW, Pinkner JS, Fremont DH, Janetka JW, et al. 2017. Selective depletion of uropathogenic E. coli from the gut by a FimH antagonist. Nature. 546(7659):528–532. doi: 10.1038/nature22972.
  • Ulrey RK, Barksdale SM, Zhou W, van Hoek ML. 2014. Cranberry proanthocyanidins have anti-biofilm properties against Pseudomonas aeruginosa. BMC Complement Altern Med. 14(1):499. doi: 10.1186/1472-6882-14-499.
  • Urena-Saborio H, Udayan APM, Alfaro-Viquez E, Madrigal-Carballo S, Reed JD, Gunasekaran S. 2021. Cranberry proanthocyanidins-pani nanocomposite for the detection of bacteria associated with urinary tract infections. Biosensors (Basel). 11(6):199. doi: 10.3390/bios11060199.
  • Valentova K, Stejskal D, Bednar P, Vostalova J, Cíhalík C, Vecerova R, Koukalova D, Kolar M, Reichenbach R, Sknouril L, et al. 2007. Biosafety, antioxidant status, and metabolites in urine after consumption of dried cranberry juice in healthy women: a pilot double-blind placebo controlled trial. J Agric Food Chem. 55(8):3217–3224. doi: 10.1021/jf0636014.
  • Vicariotto F. 2014. Effectiveness of an association of a cranberry dry extract, D-mannose, and the two microorganisms Lactobacillus plantarum LP01 and Lactobacillus paracasei LPC09 in women affected by cystitis: a pilot study. J Clin Gastroenterol. 48 Suppl 1:S96–S101.
  • Waterhouse AL, Ignelzi S, Shirley JR. 2000. A comparison of methods for quantifying oligomeric proanthocyanidins from grape seed extracts. Am J Enol Vitic. 51(4):383–389. doi: 10.5344/ajev.2000.51.4.383.
  • Weichhart T, Zlabinger GJ, Säemann MD. 2005. The multiple functions of Tamm-Horsfall protein in human health and disease: a mystery clears up. Wien Klin Wochenschr. 117(9-10):316–322. doi: 10.1007/s00508-005-0353-8.
  • Williams G, Hahn D, Stephens JH, Craig JC, Hodson EM. 2023. Cranberries  for preventing urinary tract infections. Cochrane Database Syst Rev. 4(4):CD001321.
  • Yamabhai M, Sak-Ubol S, Srila W, Haltrich D. 2016. Mannan biotechnology: from biofuels to health. Crit Rev Biotechnol. 36(1):32–42.
  • Zafriri D, Ofek I, Adar R, Pocino M, Sharon N. 1989. Inhibitory activity of cranberry juice on adherence of type 1 and type P fimbriated Escherichia coli to eucaryotic cells. Antimicrob Agents Chemother. 33(1):92–98. doi: 10.1128/AAC.33.1.92.