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Published in: BMC Complementary Medicine and Therapies 1/2017

Open Access 01-12-2017 | Research article

Phytochemical-rich foods inhibit the growth of pathogenic trichomonads

Authors: Sabrina M. Noritake, Jenny Liu, Sierra Kanetake, Carol E. Levin, Christina Tam, Luisa W. Cheng, Kirkwood M. Land, Mendel Friedman

Published in: BMC Complementary Medicine and Therapies | Issue 1/2017

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Abstract

Background

Plants produce secondary metabolites that often possess widespread bioactivity, and are then known as phytochemicals. We previously determined that several phytochemical-rich food-derived preparations were active against pathogenic foodborne bacteria. Trichomonads produce disease (trichomoniasis) in humans and in certain animals. Trichomonads are increasingly becoming resistant to conventional modes of treatment. It is of interest to test bioactive, natural compounds for efficacy against these pathogens.

Methods

Using a cell assay, black tea, green tea, grape, pomegranate, and jujube extracts, as well as whole dried jujube were tested against three trichomonads: Trichomonas vaginalis strain G3 (found in humans), Tritrichomonas foetus strain D1 (found in cattle), and Tritrichomonas foetus-like organism strain C1 (found in cats). The most effective of the test substances was subsequently tested against two metronidazole-resistant Trichomonas vaginalis strains, and on normal mucosal flora.

Results

Black tea extract inhibited all the tested trichomonads, but was most effective against the T. vaginalis organisms. Inhibition by black tea was correlated with the total and individual theaflavin content of the two tea extracts determined by HPLC. Metronidazole-resistant Trichomonas vaginalis strains were also inhibited by the black tea extract. The response of the organisms to the remaining preparations was variable and unique. We observed no effect of the black tea extract on common normal flora bacteria.

Conclusions

The results suggest that the black tea, and to a lesser degree green tea, grape seed, and pomegranate extracts might present possible natural alternative therapeutic agents to treat Trichomonas vaginalis infections in humans and the related trichomonad infections in animals, without negatively affecting the normal flora.
Literature
1.
go back to reference Kissinger P, Adamski A. Trichomoniasis and HIV interactions: a review. Sex Trans Inf. 2013;89(6):426–33.CrossRef Kissinger P, Adamski A. Trichomoniasis and HIV interactions: a review. Sex Trans Inf. 2013;89(6):426–33.CrossRef
2.
go back to reference Mostegl MM, Richter B, Nedorost N, Maderner A, Dinhopl N, Weissenböck H. Investigations on the prevalence and potential pathogenicity of intestinal trichomonads in pigs using in situ hybridization. Vet Parasitol. 2011;178(1–2):58–63.CrossRefPubMedPubMedCentral Mostegl MM, Richter B, Nedorost N, Maderner A, Dinhopl N, Weissenböck H. Investigations on the prevalence and potential pathogenicity of intestinal trichomonads in pigs using in situ hybridization. Vet Parasitol. 2011;178(1–2):58–63.CrossRefPubMedPubMedCentral
3.
5.
go back to reference Li W-C, Wang K, Zhang W, Wu J, Gu Y-F, Zhang X-C. Prevalence and molecular characterization of intestinal trichomonads in pet dogs in east China. Korean J Parasitol. 2016;54(6):703–10.CrossRefPubMedPubMedCentral Li W-C, Wang K, Zhang W, Wu J, Gu Y-F, Zhang X-C. Prevalence and molecular characterization of intestinal trichomonads in pet dogs in east China. Korean J Parasitol. 2016;54(6):703–10.CrossRefPubMedPubMedCentral
6.
go back to reference Liu J, Kanetake S, Wu Y-H, Tam C, Cheng LW, Land KM, Friedman M. Anti-protozoal effects of the tomato tetrasaccharide glycoalkaloid tomatine and the aglycone tomatidine on mucosal trichomonads. J Agric Food Chem. 2016;64(46):8806–10.CrossRefPubMed Liu J, Kanetake S, Wu Y-H, Tam C, Cheng LW, Land KM, Friedman M. Anti-protozoal effects of the tomato tetrasaccharide glycoalkaloid tomatine and the aglycone tomatidine on mucosal trichomonads. J Agric Food Chem. 2016;64(46):8806–10.CrossRefPubMed
7.
go back to reference Friedman M. Antibacterial, antiviral, and antifungal properties of wines and winery byproducts in relation to their flavonoid content. J Agric Food Chem. 2014;62(26):6025–42.CrossRefPubMed Friedman M. Antibacterial, antiviral, and antifungal properties of wines and winery byproducts in relation to their flavonoid content. J Agric Food Chem. 2014;62(26):6025–42.CrossRefPubMed
8.
go back to reference Joshi SS, Su X, D'Souza DH. Antiviral effects of grape seed extract against feline calicivirus, murine norovirus, and hepatitis a virus in model food systems and under gastric conditions. Food Microbiol. 2015;52:1–10.CrossRefPubMed Joshi SS, Su X, D'Souza DH. Antiviral effects of grape seed extract against feline calicivirus, murine norovirus, and hepatitis a virus in model food systems and under gastric conditions. Food Microbiol. 2015;52:1–10.CrossRefPubMed
9.
go back to reference Trošt K, Klančnik A, Mozetič Vodopivec B, Sternad Lemut M, Jug Novšak K, Raspor P, Smole MS. Polyphenol, antioxidant and antimicrobial potential of six different white and red wine grape processing leftovers. J Sci Food Agric. 2016;96(14):4809–20.CrossRefPubMed Trošt K, Klančnik A, Mozetič Vodopivec B, Sternad Lemut M, Jug Novšak K, Raspor P, Smole MS. Polyphenol, antioxidant and antimicrobial potential of six different white and red wine grape processing leftovers. J Sci Food Agric. 2016;96(14):4809–20.CrossRefPubMed
10.
go back to reference Yadav D, Kumar A, Kumar P, Mishra D. Antimicrobial properties of black grape (Vitis vinifera L.) peel extracts against antibiotic-resistant pathogenic bacteria and toxin producing molds. Indian J Pharmacol. 2015;47(6):663–7.CrossRefPubMedPubMedCentral Yadav D, Kumar A, Kumar P, Mishra D. Antimicrobial properties of black grape (Vitis vinifera L.) peel extracts against antibiotic-resistant pathogenic bacteria and toxin producing molds. Indian J Pharmacol. 2015;47(6):663–7.CrossRefPubMedPubMedCentral
11.
go back to reference Al-Reza SM, Bajpai VK, Kang SC. Antioxidant and antilisterial effect of seed essential oil and organic extracts from Zizyphus jujuba. Food Chem Toxicol. 2009;47(9):2374–80.CrossRefPubMed Al-Reza SM, Bajpai VK, Kang SC. Antioxidant and antilisterial effect of seed essential oil and organic extracts from Zizyphus jujuba. Food Chem Toxicol. 2009;47(9):2374–80.CrossRefPubMed
12.
go back to reference Daneshmand F, Zare-Zardini H, Tolueinia B, Hasani Z, Ghanbari T. Crude extract from Ziziphus jujuba fruits, a weapon against pediatric infectious disease. Iran J Ped Hematol Oncol. 2013;3(1):216–21.PubMedPubMedCentral Daneshmand F, Zare-Zardini H, Tolueinia B, Hasani Z, Ghanbari T. Crude extract from Ziziphus jujuba fruits, a weapon against pediatric infectious disease. Iran J Ped Hematol Oncol. 2013;3(1):216–21.PubMedPubMedCentral
13.
go back to reference Friedman M. Bioactive compounds from Ziziphus jujuba and allied species. In: Liu D, Ye X, Jiang Y, editors. Chinese dates: a traditional functional food. Boca Raton, FL: CRC Press; 2016. p. 35–52.CrossRef Friedman M. Bioactive compounds from Ziziphus jujuba and allied species. In: Liu D, Ye X, Jiang Y, editors. Chinese dates: a traditional functional food. Boca Raton, FL: CRC Press; 2016. p. 35–52.CrossRef
14.
go back to reference Juneja VK, Cadavez V, Gonzales-Barron U, Mukhopadhyay S, Friedman M. Effect of pomegranate powder on the heat inactivation of Escherichia coli O104:H4 in ground chicken. Food Control. 2016;70:26–34.CrossRef Juneja VK, Cadavez V, Gonzales-Barron U, Mukhopadhyay S, Friedman M. Effect of pomegranate powder on the heat inactivation of Escherichia coli O104:H4 in ground chicken. Food Control. 2016;70:26–34.CrossRef
15.
go back to reference Karaman S, Karasu S, Tornuk F, Toker OS, Ü G Sagdic O, N O G O. Recovery potential of cold press byproducts obtained from the edible oil industry: physicochemical, bioactive, and antimicrobial properties. J Agric Food Chem. 2015;63(8):2305–13.CrossRefPubMed Karaman S, Karasu S, Tornuk F, Toker OS, Ü G Sagdic O, N O G O. Recovery potential of cold press byproducts obtained from the edible oil industry: physicochemical, bioactive, and antimicrobial properties. J Agric Food Chem. 2015;63(8):2305–13.CrossRefPubMed
16.
go back to reference Rosas-Burgos EC, Burgos-Hernández A, Noguera-Artiaga L, Kačániová M, Hernández-García F, Cárdenas-López JL, Carbonell-Barrachina AA. Antimicrobial activity of pomegranate peel extracts as affected by cultivar. J Sci Food Agric. 2017;97(3):802–10.CrossRefPubMed Rosas-Burgos EC, Burgos-Hernández A, Noguera-Artiaga L, Kačániová M, Hernández-García F, Cárdenas-López JL, Carbonell-Barrachina AA. Antimicrobial activity of pomegranate peel extracts as affected by cultivar. J Sci Food Agric. 2017;97(3):802–10.CrossRefPubMed
17.
go back to reference Wafa BA, Makni M, Ammar S, Khannous L, Hassana AB, Bouaziz M, Es-Safi NE, Gdoura R. Antimicrobial effect of the Tunisian Nana variety Punica granatum L. extracts against Salmonella enterica (serovars Kentucky and Enteritidis) isolated from chicken meat and phenolic composition of its peel extract. Int J Food Microbiol. 2017;241:123–31.CrossRefPubMed Wafa BA, Makni M, Ammar S, Khannous L, Hassana AB, Bouaziz M, Es-Safi NE, Gdoura R. Antimicrobial effect of the Tunisian Nana variety Punica granatum L. extracts against Salmonella enterica (serovars Kentucky and Enteritidis) isolated from chicken meat and phenolic composition of its peel extract. Int J Food Microbiol. 2017;241:123–31.CrossRefPubMed
18.
go back to reference Friedman M, Mackey BE, Kim H-J, Lee I-S, Lee K-R, Lee S-U, Kozukue E, Kozukue N. Structure-activity relationships of tea compounds against human cancer cells. J Agric Food Chem. 2007;55(2):243–53.CrossRefPubMed Friedman M, Mackey BE, Kim H-J, Lee I-S, Lee K-R, Lee S-U, Kozukue E, Kozukue N. Structure-activity relationships of tea compounds against human cancer cells. J Agric Food Chem. 2007;55(2):243–53.CrossRefPubMed
19.
go back to reference Chan EW, Soh EY, Tie PP, Law YP. Antioxidant and antibacterial properties of green, black, and herbal teas of Camellia sinensis. Pharm Res. 2011;3(4):266–72. Chan EW, Soh EY, Tie PP, Law YP. Antioxidant and antibacterial properties of green, black, and herbal teas of Camellia sinensis. Pharm Res. 2011;3(4):266–72.
20.
go back to reference Friedman M. Overview of antibacterial, antitoxin, antiviral, and antifungal activities of tea flavonoids and teas. Mol Nutr Food Res. 2007;51(1):116–34.CrossRefPubMed Friedman M. Overview of antibacterial, antitoxin, antiviral, and antifungal activities of tea flavonoids and teas. Mol Nutr Food Res. 2007;51(1):116–34.CrossRefPubMed
21.
go back to reference Friedman M, Henika PR, Levin CE, Mandrell RE, Kozukue N. Antimicrobial activities of tea catechins and theaflavins and tea extracts against Bacillus cereus. J Food Prot. 2006;69(2):354–61.CrossRefPubMed Friedman M, Henika PR, Levin CE, Mandrell RE, Kozukue N. Antimicrobial activities of tea catechins and theaflavins and tea extracts against Bacillus cereus. J Food Prot. 2006;69(2):354–61.CrossRefPubMed
22.
go back to reference Juneja VK, Bari ML, Inatsu Y, Kawamoto S, Friedman M. Control of Clostridium perfringens spores by green tea leaf extracts during cooling of cooked ground beef, chicken, and pork. J Food Prot. 2007;70(6):1429–33.CrossRefPubMed Juneja VK, Bari ML, Inatsu Y, Kawamoto S, Friedman M. Control of Clostridium perfringens spores by green tea leaf extracts during cooling of cooked ground beef, chicken, and pork. J Food Prot. 2007;70(6):1429–33.CrossRefPubMed
23.
go back to reference Juneja VK, Bari ML, Inatsu Y, Kawamoto S, Friedman M. Thermal destruction of Escherichia coli O157:H7 in sous-vide cooked ground beef as affected by tea leaf and apple skin powders. J Food Prot. 2009;72(4):860–5.CrossRefPubMed Juneja VK, Bari ML, Inatsu Y, Kawamoto S, Friedman M. Thermal destruction of Escherichia coli O157:H7 in sous-vide cooked ground beef as affected by tea leaf and apple skin powders. J Food Prot. 2009;72(4):860–5.CrossRefPubMed
24.
go back to reference Bailey RG, McDowell I, Nursten HE. Use of an HPLC photodiode-array detector in a study of the nature of a black tea liquor. J Sci Food Agric. 1990;52(4):509–25.CrossRef Bailey RG, McDowell I, Nursten HE. Use of an HPLC photodiode-array detector in a study of the nature of a black tea liquor. J Sci Food Agric. 1990;52(4):509–25.CrossRef
25.
go back to reference Fischer UA, Carle R, Kammerer DR. Identification and quantification of phenolic compounds from pomegranate (Punica granatum L.) peel, mesocarp, aril and differently produced juices by HPLC-DAD-ESI/MSn. Food Chem. 2011;127(2):807–21.CrossRefPubMed Fischer UA, Carle R, Kammerer DR. Identification and quantification of phenolic compounds from pomegranate (Punica granatum L.) peel, mesocarp, aril and differently produced juices by HPLC-DAD-ESI/MSn. Food Chem. 2011;127(2):807–21.CrossRefPubMed
26.
go back to reference Choi S-H, Ahn J-B, Kozukue N, Levin CE, Friedman M. Distribution of free amino acids, flavonoids, total phenolics, and antioxidative activities of jujube (Ziziphus jujuba) fruits and seeds harvested from plants grown in Korea. J Agric Food Chem. 2011;59(12):6594–604.CrossRefPubMed Choi S-H, Ahn J-B, Kozukue N, Levin CE, Friedman M. Distribution of free amino acids, flavonoids, total phenolics, and antioxidative activities of jujube (Ziziphus jujuba) fruits and seeds harvested from plants grown in Korea. J Agric Food Chem. 2011;59(12):6594–604.CrossRefPubMed
27.
go back to reference Kuhnert N. Unraveling the structure of the black tea thearubigins. Arch Biochem Biophys. 2010;501(1):37–51.CrossRefPubMed Kuhnert N. Unraveling the structure of the black tea thearubigins. Arch Biochem Biophys. 2010;501(1):37–51.CrossRefPubMed
28.
go back to reference Radunić M, Jukić Špika M, Goreta Ban S, Gadže J, Díaz-Pérez JC, Maclean D. Physical and chemical properties of pomegranate fruit accessions from Croatia. Food Chem. 2015;177:53–60.CrossRefPubMed Radunić M, Jukić Špika M, Goreta Ban S, Gadže J, Díaz-Pérez JC, Maclean D. Physical and chemical properties of pomegranate fruit accessions from Croatia. Food Chem. 2015;177:53–60.CrossRefPubMed
29.
go back to reference Ambigaipalan P, de Camargo AC, Shahidi F. Identification of phenolic antioxidants and bioactives of pomegranate seeds following juice extraction using HPLC-DAD-ESI-MSn. Food Chem. 2017;221:1883–94.CrossRefPubMed Ambigaipalan P, de Camargo AC, Shahidi F. Identification of phenolic antioxidants and bioactives of pomegranate seeds following juice extraction using HPLC-DAD-ESI-MSn. Food Chem. 2017;221:1883–94.CrossRefPubMed
30.
go back to reference Sirk TW, Brown EF, Friedman M, Sum AK. Molecular binding of catechins to biomembranes: relationship to biological activity. J Agric Food Chem. 2009;57(15):6720–8.CrossRefPubMed Sirk TW, Brown EF, Friedman M, Sum AK. Molecular binding of catechins to biomembranes: relationship to biological activity. J Agric Food Chem. 2009;57(15):6720–8.CrossRefPubMed
31.
go back to reference Sirk TW, Brown EF, Sum AK, Friedman M. Molecular dynamics study on the biophysical interactions of seven green tea catechins with lipid bilayers of cell membranes. J Agric Food Chem. 2008;56(17):7750–8.CrossRefPubMed Sirk TW, Brown EF, Sum AK, Friedman M. Molecular dynamics study on the biophysical interactions of seven green tea catechins with lipid bilayers of cell membranes. J Agric Food Chem. 2008;56(17):7750–8.CrossRefPubMed
32.
go back to reference Sirk TW, Friedman M, Brown EF. Molecular binding of black tea theaflavins to biological membranes: relationship to bioactivities. J Agric Food Chem. 2011;59(8):3780–7.CrossRefPubMed Sirk TW, Friedman M, Brown EF. Molecular binding of black tea theaflavins to biological membranes: relationship to bioactivities. J Agric Food Chem. 2011;59(8):3780–7.CrossRefPubMed
33.
go back to reference Friedman M, Levin CE, Choi S-H, Kozukue E, Kozukue N. HPLC analysis of catechins, theaflavins, and alkaloids in commercial teas and green tea dietary supplements: comparison of water and 80% ethanol/water extracts. J Food Sci. 2006;71(6):C328–37.CrossRef Friedman M, Levin CE, Choi S-H, Kozukue E, Kozukue N. HPLC analysis of catechins, theaflavins, and alkaloids in commercial teas and green tea dietary supplements: comparison of water and 80% ethanol/water extracts. J Food Sci. 2006;71(6):C328–37.CrossRef
34.
go back to reference Friedman M, Kim S-Y, Lee S-J, Han G-P, Han J-S, Lee K-R, Kozukue N. Distribution of catechins, theaflavins, caffeine, and theobromine in 77 teas consumed in the United States. J Food Sci. 2005;70(9):C550–9.CrossRef Friedman M, Kim S-Y, Lee S-J, Han G-P, Han J-S, Lee K-R, Kozukue N. Distribution of catechins, theaflavins, caffeine, and theobromine in 77 teas consumed in the United States. J Food Sci. 2005;70(9):C550–9.CrossRef
35.
go back to reference Friedman M, Levin CE, Lee S-U, Kozukue N. Stability of green tea catechins in commercial tea leaves during storage for 6 months. J Food Sci. 2009;74(2):H47–51.CrossRefPubMed Friedman M, Levin CE, Lee S-U, Kozukue N. Stability of green tea catechins in commercial tea leaves during storage for 6 months. J Food Sci. 2009;74(2):H47–51.CrossRefPubMed
36.
go back to reference Adams M, de Kock C, Smith PJ, Land KM, Liu N, Hopper M, Hsiao A, Burgoyne AR, Stringer T, Meyer M, et al. Improved antiparasitic activity by incorporation of organosilane entities into half-sandwich ruthenium(II) and rhodium(III) thiosemicarbazone complexes. Dalton Trans. 2015;44(5):2456–68.CrossRefPubMed Adams M, de Kock C, Smith PJ, Land KM, Liu N, Hopper M, Hsiao A, Burgoyne AR, Stringer T, Meyer M, et al. Improved antiparasitic activity by incorporation of organosilane entities into half-sandwich ruthenium(II) and rhodium(III) thiosemicarbazone complexes. Dalton Trans. 2015;44(5):2456–68.CrossRefPubMed
37.
go back to reference Stringer T, Taylor D, Guzgay H, Shokar A, Au A, Smith PJ, Hendricks DT, Land KM, Egan TJ, Smith GS. Polyamine quinoline rhodium complexes: synthesis and pharmacological evaluation as antiparasitic agents against Plasmodium falciparum and Trichomonas vaginalis. Dalton Trans. 2015;44(33):14906–17.CrossRefPubMed Stringer T, Taylor D, Guzgay H, Shokar A, Au A, Smith PJ, Hendricks DT, Land KM, Egan TJ, Smith GS. Polyamine quinoline rhodium complexes: synthesis and pharmacological evaluation as antiparasitic agents against Plasmodium falciparum and Trichomonas vaginalis. Dalton Trans. 2015;44(33):14906–17.CrossRefPubMed
38.
go back to reference Nisha KK, Bhargava G, Land KM, Chang KH, Arora R, Sen S, Kumar V. N-Propargylated isatin-Mannich mono- and bis-adducts: synthesis and preliminary analysis of in vitro activity against Tritrichomonas foetus. Eur J Med Chem. 2014;74:657–63.CrossRefPubMed Nisha KK, Bhargava G, Land KM, Chang KH, Arora R, Sen S, Kumar V. N-Propargylated isatin-Mannich mono- and bis-adducts: synthesis and preliminary analysis of in vitro activity against Tritrichomonas foetus. Eur J Med Chem. 2014;74:657–63.CrossRefPubMed
39.
go back to reference Stringer T, Taylor D, de Kock C, Guzgay H, Au A, An SH, Sanchez B, O'Connor R, Patel N, Land KM, et al. Synthesis, characterization, antiparasitic and cytotoxic evaluation of thioureas conjugated to polyamine scaffolds. Eur J Med Chem. 2013;69:90–8.CrossRefPubMed Stringer T, Taylor D, de Kock C, Guzgay H, Au A, An SH, Sanchez B, O'Connor R, Patel N, Land KM, et al. Synthesis, characterization, antiparasitic and cytotoxic evaluation of thioureas conjugated to polyamine scaffolds. Eur J Med Chem. 2013;69:90–8.CrossRefPubMed
40.
go back to reference Setzer MS, Byler KG, Ogungbe IV, Setzer WN. Natural products as new treatment options for trichomoniasis: a molecular docking investigation. Sci Pharm. 2017;85(1):5.CrossRefPubMedCentral Setzer MS, Byler KG, Ogungbe IV, Setzer WN. Natural products as new treatment options for trichomoniasis: a molecular docking investigation. Sci Pharm. 2017;85(1):5.CrossRefPubMedCentral
Metadata
Title
Phytochemical-rich foods inhibit the growth of pathogenic trichomonads
Authors
Sabrina M. Noritake
Jenny Liu
Sierra Kanetake
Carol E. Levin
Christina Tam
Luisa W. Cheng
Kirkwood M. Land
Mendel Friedman
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2017
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-017-1967-x

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