Mechanism of action of cranberry in preventing urinary tract infections

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1 Mechanism of action of cranberry in preventing urinary tract infections Further to a description of the pathophysiology of urinary tract infections (UTIs) of the uroepithelial cells by Escherichia coli (E. coli), the mechanism of action of cranberry in the prevention of UTIs, especially recurrent UTIs (rutis), will be presented in this paper. 1. Therapeutic approach to the treatment of urinary tract infections caused by Escherichia. coli The human body uses very straightforward mechanisms of defense against the adhesion of bacteria such as urinary slime, also known as uromodulin or Tamm-Horsfall glycoprotein. This glycoprotein is produced by the kidneys and excreted in great quantities in the urine. Escherichia coli as well other bacteria bind to it strongly which results in them being flushed out of the human body. Similar results have been noted after the administration of D-mannose, which imitates the mannose moieties to which E. coli structures are sensitive. This results in the bacterium being trapped Antibiotic treatment and antimicrobial resistance (AMR) Despite the growing concern related to the development of antibiotic resistance 1 and the problem of recurrent UTIs, antibiotics are the usual first line treatment for urinary tract infections. Antibiotics interact with the bacteria and significantly interfere with one or more of its physiological metabolic pathways resulting in the death of the bacteria. Drugs commonly recommended include trimethoprim, sulfamethoxazole (Bactrim), fosfomycin (Monurol) and nitrofurantoin (Macrodantin, Macrobid). Example: trimethoprim, sulfamethoxazole Sulfamethoxazole interferes with the intracellular synthesis of folate inside microbial organisms (such as protozoa, fungi and bacteria) by competing with the natural substrate p-aminobenzoic acid (PABA) in the biosynthesis of dihydrofolate. Trimethoprim serves as a competitive inhibitor of dihydrofolate reductase (DHFR), which inhibits the intracellular synthesis of tetrahydrofolate. The effect is bactericidal and irreversible. 1 A study on Mexican women showed that E.coli present in more than 50% of them were resistant to the most common antibiotics.

2 1.2. Use of cranberry in UTIs treatment and prevention Cranberry has been shown effective in many cases in preventing UTIs, especially recurrent urinary tract infections (rutis) by inhibiting adhesion. The constituents of cranberry include flavonoids, anthocyanidins, and proanthocyanidins. In the natural environment, anthocyanidins and proanthocyanidins protect the plant from infections through their anti-adhesion properties. Authors have noted that cranberry juice cocktail consumption protected against P-fimbriated E. coli against both sensitive and resistant strains, with a mechanism that is not likely to increase resistance 2. In fact, resistance has been seen in antibiotic treatment 3 and not in cranberry intake even for 12 months 4, 5. Not increasing resistance is a sign that there is no significant modification of a metabolic pathway of the bacterium. Cranberry works on multi-resistant strains Evaluation of the pharmacological or non-pharmacological nature of Cranberry s antiadhesive mechanism of action 2.1. Mechanism of action of cranberry in preventing E.coli adherence From cranberry, reducing E.coli infection of the urinary tract is achieved through a mechanism other than killing bacteria. E.coli infections come from fecal E.coli, or from catheters, which immediately become infested with E.coli biofilm. The mechanism exerted by cranberry is similar to the one physiologically proposed by the organism: hindering bacterial binding to urinary epithelium thus promoting its elimination in the urinary flow. The organism achieves such an antiadhesive activity by secreting in the urine substances which bind to bacteria so that bacteria cannot bind to the uroepithelium 7, 8. The characteristics which allow E.coli to bind to uroepithelium or to abiotic surfaces (such as plastics) are as follows: the presence of lipids and carbohydrates (from LPS or extracellular matrix carbohydrates) which attract other surfaces through non-specific interactions (van der Waals forces, H-bonds, hydrophobic interactions), and 2 Howell A. JAMA 2002 (287) 23 p Cranberry Juice and Adhesion of Antibiotic-Resistant Uropathogens. 3 Williams G 2011 Cochrane Database Syst Rev.Mar 16;(3):Long-term antibiotics for preventing recurrent urinary tract infection in children. 4 Beerepoot Arch Intern Med. 2011;171(14): Cranberries vs Antibiotics to Prevent Urinary Tract Infections A Randomized Double-blind Noninferiority Trial in Premenopausal Women 5 Jepson RG Cochrane Database Syst Rev Cranberries for preventing urinary tract infections (Review) 6 Gupta A Urol Res 2012 (40) pp Inhibition of adherence of multi drug resistant E.coli by proanthocyanidin 7 Parkkinen J 1988 Infection and Immunity (56) 10 pp Identification of factors in human urine that inhibit the binding of E.coli adhesins 8 Weichhart T. Eur J Clin invest 2008 (38) S2 pp Current concepts of molecular defence mechanisms operative during urinary tract infection 2

3 the presence of appendages such as fimbriae which have affinity for specific hydrophilic carbohydrate ligands (Type I fimbriae mannose, galactose). The characteristics of the interaction of cranberry with E.coli are further explained in the following paragraphs Mitigation of non-specific interactions The interactions between E.coli and a surface (uroepithelial cell or abiotic surfaces) involves many types of non-specific interactions such as Van der Waal forces, hydrogen bonds and hydrophobic interactions 9, 10, 11. These forces have a different role depending on the type of E.coli, on the type and quantity of Lipopolysaccharide (LPS) stemming from its cell wall, depending on whether the bacterium is or is not fimbriated and on the type of fimbriae. Typically van der Waals forces (dipole-dipole) and hydrogen bonds are expressed at medium distance from the surface; hydrophobic forces, acting between bacterial lipids and the lipids of the cell or other hydrophobic elements of the plastic surface, take place at small distances. There is evidence that these forces may change depending on the environment 12 (ionic force, polarity of the medium, ph) in the direction of increasing as much as possible the possibility of E.coli to adhere to the surface and colonize it. Proanthocyanidins are very big oligomers and have hydrophobic aromatic skeleton, with hydrophilic hydroxyl and carboxyl residues, (-OH and COOH) and therefore can interact with both hydrophobic and hydrophilic elements of the bacterium. In fact, addition of a biological surfactant (rhamnolipid) decreases tannin activity in experiments with Pseudomonas. aeruginosa 13. All experiments conducted show that cranberry juice decreases hydrophobicity 14, thus decreasing the opportunity for short-range interactions, as well as reducing all other nonspecific interactions 15. In addition, specific research conducted on the interactions between bacteria and abiotic plastic surfaces in absence and in presence of cranberry juice showed that the reduction of adherence due to cranberry is very strong and very non-specific because it is exerted towards very different situations, including completely non biologic surfaces, as listed below. 9 Johnson-White 2006 Anal Chem (78) Prevention of nonspecific bacterial cell adhesion in immunoassays by use of cranberry juice 10 Wojnicz D et al 2012 Phytomedicine (19) Study on the influence of cranberry extract Zuravit S.O.S on the properties of 11 Schneider P et al Epidemiol Infect 1991 (106) Cell-surface hydrophobicity of Staphylococcus saprophyticus 12 Abu-Lail N 2006 Colloids and Surfaces B: Biointerfaces (51) The effect of solvent polarity on the molecular surface properties and adhesion of E.coli. 13 O May et al 2011 App and Env Microb (77) 9 pp The swarming motility of P. aeruginosa is blocked by cranberry proanthocyanidins and other tannin containing materials. 14 Uberos 2011 Microbiology insights (4) Cranberry (Vaccinum macrocarpon) changes the surface hydrophobicity and biofilm formation of E.coli 15 Liu Y et al 2008 Colloids and Surfaces (65) Cranberry changes the physicochemical surface properties of E.coli and adhesion with uroepithelial cells 3

4 Evidence showed that 16, 17 adherence reduction was expressed to different organisms, both G+ (Enterobacter faecalis) and G- (E.coli); adherence reduction was expressed towards both uroepithelial cells and abiotic surfaces (plastic, glass, a silicon nitrate probe); adherence reduction was similarly expressed towards two non-biological surfaces : latex and plastic; Inhibition of adherence is not directly proportional to concentration: it greatly decreases at higher concentrations in an exponential rather than a linearly proportional trend. The mechanism which is involved in these results is steric interactions (steric stabilization, steric hindrance): the cranberry proanthocianidins interact in a non-specific way with particles (E.coli or latex) due to non-specific bonding and trap the substance in a rigid structure. After PAC has englobed E.coli, there is no room for interaction with other surfaces, such as a uroepithelial cell or a plastic surface. Steric stabilization is a well-known phenomenon of colloid literature. Adsorbed layers of polymer (such as cranberry derived PAC) on surfaces of biocolloids (e.g. bacteria) or collector surfaces (e.g. plastic material used in catheters) can give rise to steric interactions upon approach of the bacterial cell to the biomaterial surface. This steric hindrance constitutes a very high energy barrier which impedes further approach and adhesion to any surface. This steric interaction explains why A-linked PACS are necessary with respect to B-linked: they are more rigid 18. This rigidity allows steric hindrance to be most effective Fimbriae motility or length The presence of fimbriae gives another possibility to bonding due to ligand-specific spots. These ligand spots are carbohydrate moieties on uroepithelial cells and hydrophilic spots on abiotic surfaces. Free fimbriae aim to bind to the binding spot in order to assure resistance to urine flow and to other types of repulsion, drawing the bacterial cell near to the surface in order to promote non-specific long and short radius interactions. It has been observed that Cranberry extract decreased motility by presence of cranberry extract without suppressing the process of fimbriation of E.coli 19 ; 16 Eydelnant et al 2008 Langmuir (24) Cranberry derived proanthocyanidins reduce bacterial adhesion to selected biomaterials 17 Wojnicz D et al 2012 Phytomedicine (19) Study on the influence of cranberry extract Zuravit S.O.S on the properties of 18 Howell A et al Phytochemistry 2005 (66) A-type cranberry proanthocyanidins and uropathogenic bacterial anti-adhesion activity. 19 Wojnicz D et al 2012 Phytomedicine (19) Study on the influence of cranberry extract Zuravit S.O.S on the properties of 4

5 Cranberry extract provoked a decrease in P-fimbriae length of E.coli HB101 pdc1 (P-fimbriated E.coli strain) which resulted in a reduced adhesion of P-fimbriated E.coli to silver nitrate probe 20, 21 ; Cranberry extract decreased swarming but not swimming or twitching in P.aeruginosa 22, All effects were reversible and conformation returned same as control when cranberry was removed 23 ; There was no bacteriostatic or bactericidal action from cranberry 24. These phenomena are due to conformational changes, meaning that the fimbriae were more compressed on the bacterial surface in the presence of cranberry. These changes reached quickly a plateau. This conformational change was completely reversible when the solution was placed into water, showing a physical interaction with the fimbriae and not a genetical modification or suppression of the fimbriae synthesis. Steric interactions also explain cranberry inhibition fimbral mediated adhesion Evidence of a non-pharmacological mode of action of cranberry antiadhesion on E.coli It is necessary to observe and discuss the characteristics of the anti-adhesion mechanism of action of cranberry in order to evaluate whether it is pharmacological or not. There is no evidence of a pharmacological mode of action for the anti-adhesion activity of cranberry. Evidences than the mode of action is not pharmacological are listed below Heterogeneous constituents are responsible for the action A-linked proanthocyanidins (A-PACS) have been shown to be involved in the therapeutic effect 25. The A-PACs are a class of highly heterogeneous substances of 4-10 units of polyflavan-3-ols oligomers based on a repeating structure of epicatechin with one or more A-type interflavanyl linkages present in the oligomer. The A-linkage gives a greater conformational rigidity to the substances 26. This rigidity is probably responsible for steric hindrance, which means having a greater efficacy to the trapping potential of bacteria. 20 Liu Y et al 2008 Colloids and Surfaces (65) Cranberry changes the physicochemical surface properties of E.coli and adhesion with uroepithelial cells 21 Pinzon-Arango P et al 2009 J Med Food (12) 2 pp Role of cranberry on bacterial adhesion forces and implications for E.coli uroepithelial cell attachment 22 O May et al 2011 App and Env Microb (77) 9 pp The swarming motility of P. aeruginosa is blocked by cranberry proanthocyanidins and other tannin containing materials. 23 Liu Y et al 2006 Biot and Bioeng (93) 2 pp Role of cranberry juice on molecular scale surface characteristics and adhesion behavior of E.coli 24 Sobota AE 1984 The Journal of Urology (131) 5 pp Inhibition of bacterial adherence by cranberry juice: potential use for the treatment of urinary tract infections. 25 Foo L et al Phytochemistry 2000 (54) Foo L et al Phytochemistry 2000 (54) Howell A et al Phytochemistry 2005 (66) A-type cranberry proanthocyanidins and uropathogenic bacterial anti-adhesion activity. 5

6 In the Zuravit product, tested in an article indicated by CA 11, the proanthocyanidin content was: 21% monomeric, 49% dimeric, 30 % trimeric forms of proanthocyanidins, showing an interaction which implies chemical-physical characteristics and not pharmacological atom-specific interactions 27. In addition, cranberry extracts have shown greater performance than A-PACS, showing that performance is reached by multiple components. These resemble the chemical physical mechanism put in place by the organism to hinder interaction, which does not involve receptors linked to any pharmacological pathway Reversibility The antiadhesive effects of cranberry are reversible, and bacteria regrown in cranberry-free medium retrieved their ability to attach to uroepithelium, and their adhesion forces reverted to the values observed in the control sample 29. Any conformational change in fimbriae is reversible, in contrast with the hypotheses that anthocyanidins may reduce the expression of fimbriae at the genetic level, as expressed by earlier authors and corroborates the physical chemical interaction 30. The action of cranberry is neither bactericidal nor bacteriostatic Action on resistant strains and resistance-risk due to cranberry Based on studies noted hereunder, authors have noted that the consumption of cranberry products protected against both sensitive and resistant strains P-fimbriated E. coli. The authors also remarked that the mechanism of action was one that is not likely to increase resistance 32. In fact, resistance has been seen in antibiotic treatment 33 and not in cranberry intake even for 12 months 34, 35. Not increasing resistance is a sign that there is no significant modification of a metabolic pathway of the bacterium. Cranberry works on multi-resistant strains Wojnicz D et al 2012 Phytomedicine (19) Study on the influence of cranberry extract Zuravit S.O.S on the properties of 28 Pinzon-Arango P et al Food Sci Biotechnol 2011 (20) 5 Impact of cranberry Juice and proantocyanidins on the ability of E. coli to form biofilms Pinzon-Arango P et al Food Sci Biotechnol 2011 (20) 5 Impact of cranberry Juice and proantocyanidins on the ability of E. coli to form biofilms Wojnicz D et al 2012 Phytomedicine (19) Study on the influence of cranberry extract Zuravit S.O.S on the properties of 31 Sobota AE 1984 Inhibition of bacterial adherence by cranberry juice: potential use for the treatment of urinary tract infections. 32 Howell A. JAMA 2002 (287) 23 p Cranberry Juice and Adhesion of Antibiotic-Resistant Uropathogens. 33 Williams G 2011 Cochrane Database Syst Rev.Mar 16;(3):Long-term antibiotics for preventing recurrent urinary tract infection in children. 34 Beerepoot Arch Intern Med. 2011;171(14): Cranberries vs Antibiotics to Prevent Urinary Tract Infections A Randomized Double-blind Noninferiority Trial in Premenopausal Women 35 Jepson RG Cochrane Database Syst Rev Cranberries for preventing urinary tract infections (Review) 36 Gupta A Urol Res 2012 (40) pp inhibition of adherence of multi drug resistant E.coli by proanthocyanidin 6

7 Heterogeneity of microorganisms influenced by cranberry Cranberry can be used in preventing the adhesion of different microorganisms, including both gram positive (G+) and gram negative (G-) bacteria and yeasts such as Candida. Escherichia coli with fimbriae (urinary tract) Streptococcus mutans (oral cavity) 39 Helicobacter pylori (stomach) 37 Candida albicans (genito-urinary tract, oral) 40 Pseudomonas auriginosa (urinary tract) 38. Haemophilus influenzae (upper respiratory tract) Johnson-White 2006 Anal Chem (78) Prevention of nonspecific bacterial cell adhesion in immunoassays by use of cranberry juice 38 O May et al 2011 App and Env Microb (77) 9 pp The swarming motility of P. aeruginosa is blocked by cranberry proanthocyanidins and other tannin containing materials. 39 Shmuely H 2012 Curr Opin Biotechnol. (23) 2 pp: Cranberry components for the therapy of infectious disease. 40 Feldman 2012 Feldman et al. BMC Complementary and Alternative Medicine, 12:6 Cranberry proanthocyanidins inhibit the adherence properties of Candida albicans and cytokine secretion by oral epithelial cells 41 Shmuely H 2012 Curr Opin Biotechnol. (23) 2 pp: Cranberry components for the therapy of infectious disease. 7

8 Action expressed in abiotic environment and no interaction with the body The cranberry extracts do not interact with the cells of the host in order to prevent adhesion: Urine collected from people to whom cranberry is administrated inhibits adhesion on abiotic surfaces, showing that the action is carries out in the urine and is not exerted on uroepithelial cells. Cranberry prevents adhesion of E.coli to silicone probe, to glass or plastic such as Polyvinyl chloride (PVC), showing no interaction with the uroepithelial cell 42 Cranberry prevents adhesion on completely abiotic substrata: it inhibits adhesion of latex to plastic thus eliminating any doubt of any pharmacologically mediated action 43. Microscope images (20x magnification) Polytethrafluoroethylene surface following flow experiments with latex microspheres (a) in the absence of PAC (control condition) and b) in the presence of PAC (Eydelnant, Langmuir 2008) a) b) The mechanism of action of cranberry is to bind to the E.coli inside the lumen of the ureter, bladder and urethra so as to exert steric hindrance on the bacterial cell which inhibits adhesion by non-specific interactions. In addition, cranberry exerts steric hindrance on fimbriae (both P and type 1) resulting in conformational changes in the fimbria that do not make the fimbria available for specific ligand binding to either uroepithelial cells or abiotic surfaces (e.g. catheters). Since adherence is the first step to biofilm formation and/or infection, hindering adherence is a fundamental step to inhibiting infection. The mechanism of action is not pharmacological, metabolic or immunological. 42 Pinzon-Arango P et al Food Sci Biotechnol 2011 (20) 5 Impact of cranberry Juice and proanthocyanidins on the ability of E. coli to form biofilms Eydelnant et al 2008 Langmuir (24) Cranberry derived proanthocyanidins reduce bacterial adhesion to selected biomaterials

9 The non-pharmacological mechanism of action of cranberry makes it a very interesting substance in cases where recurring UTIs are due to resistant bacteria. Preventive treatment could also be done in case of catheterization. UTIs with resistant bacteria and from catheters are already an emergency. 3. Conclusions The pharmacological mode of action would imply an interaction with a receptor directly connected with a biological pathway which significantly modifies a physiological response; in other words, it would imply a specific interaction with a receptor which is directly connected with a mechanism of transduction of the signal. Considering the characteristics of the mechanism of action of cranberry products drawing from all the major literature on the subject, the following is of note: 1. Cranberry prevents E. coli adhesion by binding to it, thus hindering the non-specific adhesion and the ligand-specific fimbrial adhesion to uroepithelial cell or other surfaces through electric and steric hindrance. 2. The components of cranberry are A-PACs together with other constituents. A-PACS are a heterogeneous group of substances characterized by an A-linkage which confers rigidity to the compound. 3. The action of cranberry is reversible, causing no death or significant modification of metabolism of the bacterium. 4. The interaction between cranberry and micro-organisms is biologically aspecific since it hinders different sorts of microbes from adhering to the host including Gram negative bacteria such as Escherichia coli, Helicobacter pylori, Haemophilus influenzae and Gram positive bacteria such as Streptococcus mutans, and Enterobacter. faecalis. 5. Cranberry works with a mechanism which does not create resistance. 6. Cranberry has an action on multi-drug resistant bacteria. 7. Cranberry does not need to interact with the uroepithelial tissue not with bacteria, showing that the anti-adhesion properties are not mediated by any influence of cellular pharmacological pathways. Therefore, it can be concluded that cranberry products whose mode of action depends on proanthocyanidins do not achieve the treatment and prevention effects for a UTI by pharmacological, immunological or metabolic means. 9

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