Characterization of polyphenolic constituents from Sanguisorba officinalis L. and its antibacterial activity

  • Hong-lin Zhu
  • Gang ChenEmail author
  • Sun-ni Chen
  • Qi-rui Wang
  • Ling Wan
  • Su-ping Jian
Original Paper


Sanguisorba officinalis L., one kind of perennial plants, has been widely distributed in southern Europe, northern Africa and China. The objective of the present work was to evaluate the antibacterial captivities of polyphenolic extract (PE) of S. officinalis L. on five pathogenic bacteria, including Gram-negative bacteria (Escherichia coli and Salmonella typhimurium) and Gram-positive bacteria (Staphylococcus aureus, Listeria monocytogenes and Bacillus subtilis). The antibacterial activities were determined by the diameter of inhibition zone, minimum inhibitory concentration and minimum bactericidal concentration tests. The results showed that purified PE had significantly better performance in inhibiting bacteria than crude PE (P < 0.05), and PE had better inhibition effect on Gram-positive bacteria than Gram-negative bacteria. Using LC–ESI–QTOF–MS/MS technology, a total of 44 polyphenolic compounds were tentatively identified, 26 of which have been discussed for the first time in S. officinalis L. Gallic acid, ellagic acid, catechin and their derivatives, which have been identified as antibacterial bioactivities previously, were the major constituents with the amounts of 10, 8 and 11, respectively. Besides, compared with potassium sorbate and sodium benzoate, purified PE with a low concentration had significantly stronger antibacterial ability against all the tested bacteria (P < 0.05), suggesting that purified PE of S. officinalis L. could be a promising source of food preservatives.


Sanguisorba officinalis L. Polyphenolic extract Antibacterial ability LC–ESI–QTOF–MS/MS 



We offer our special thanks to Qi-ying Mai and Jing-fang Li for the support of skillful technology about LC–MS, to Long Chen and Hui Xue for the technical assistance with microbiology, and to Ying-xue Du and Juan Li for revising manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interest.

Compliance with ethics requirements

This research does not contain any studies with human participants or animals performed by any of the authors.


  1. 1.
    Abdel-Aziz SM, Asker MM, Keera AA, Mahmoud MG (2016) Microbial food spoilage: control strategies for shelf life extension. Microbes in food and health. In: Garg N, Abdel-Aziz SM, Aeron A (eds) Springer. Switzerland, Cham, pp 239–264Google Scholar
  2. 2.
    da Cruz Cabral L, Pinto VF, Patriarca A (2013) Application of plant derived compounds to control fungal spoilage and mycotoxin production in foods. Int J Food Microbiol 166(1):1–14Google Scholar
  3. 3.
    De Buyser M-L, Dufour B, Maire M, Lafarge V (2001) Implication of milk and milk products in food-borne diseases in France and in different industrialised countries. Int J Food Microbiol 67(1–2):1–17PubMedGoogle Scholar
  4. 4.
    Zhao C, Ge B, De Villena J, Sudler R, Yeh E, Zhao S, White DG, Wagner D, Meng J (2001) Prevalence of Campylobacter spp., Escherichia coli, and Salmonella serovars in retail chicken, turkey, pork, and beef from the Greater Washington, DC, area. Appl Environ Microbiol 67(12):5431–5436PubMedPubMedCentralGoogle Scholar
  5. 5.
    Jemmi T, Stephan R (2006) Listeria monocytogenes: food-borne pathogen and hygiene indicator. Rev Sci Tech 25(2):571–580PubMedGoogle Scholar
  6. 6.
    Matarante A, Baruzzi F, Cocconcelli PS, Morea M (2004) Genotyping and toxigenic potential of Bacillus subtilis and Bacillus pumilus strains occurring in industrial and artisanal cured sausages. Appl Environ Microbiol 70(9):5168–5176PubMedPubMedCentralGoogle Scholar
  7. 7.
    Kadariya J, Smith TC, Thapaliya D (2014) Staphylococcus aureus and staphylococcal food-borne disease: an ongoing challenge in public health. BioMed Res Int 2014:827965PubMedPubMedCentralGoogle Scholar
  8. 8.
    Tian J, Zeng X, Feng Z, Miao X, Peng X, Wang Y (2014) Zanthoxylum molle Rehd. essential oil as a potential natural preservative in management of Aspergillus flavus. Ind Crops Prod 60:151–159Google Scholar
  9. 9.
    Diao M, Qi D, Xu M, Lu Z, Lv F, Bie X, Zhang C, Zhao H (2018) Antibacterial activity and mechanism of monolauroyl–galactosylglycerol against Bacillus cereus. Food Control 85:339–344Google Scholar
  10. 10.
    Ullah N, Parveen A, Bano R, Zulfiqar I, Maryam M, Jabeen S, Liaqat A, Ahmad S (2016) In vitro and in vivo protocols of antimicrobial bioassay of medicinal herbal extracts: a review. Asian Pac J Trop Dis 6(8):660–667. Google Scholar
  11. 11.
    Bendahou M, Muselli A, Grignon-Dubois M, Benyoucef M, Desjobert J-M, Bernardini A-F, Costa J (2008) Antimicrobial activity and chemical composition of Origanum glandulosum Desf. essential oil and extract obtained by microwave extraction: comparison with hydrodistillation. Food Chem 106(1):132–139. Google Scholar
  12. 12.
    Naidu A (2000) Natural food antimicrobial systems. CRC Press, Boca RatonGoogle Scholar
  13. 13.
    Zhang Y, Liu X, Wang Y, Jiang P, Quek S (2016) Antibacterial activity and mechanism of cinnamon essential oil against Escherichia coli and Staphylococcus aureus. Food Control 59:282–289. Google Scholar
  14. 14.
    Diao W-R, Hu Q-P, Zhang H, Xu J-G (2014) Chemical composition, antibacterial activity and mechanism of action of essential oil from seeds of fennel (Foeniculum vulgare Mill.). Food Control 35(1):109–116. Google Scholar
  15. 15.
    Lv F, Liang H, Yuan Q, Li C (2011) In vitro antimicrobial effects and mechanism of action of selected plant essential oil combinations against four food-related microorganisms. Food Res Int 44(9):3057–3064. Google Scholar
  16. 16.
    Hara-Kudo Y, Kobayashi L, Sugita-Konishi Y, Kondo K (2004) Antibacterial activity of plants used in cooking for aroma and taste. J Food Prot 67(12):2820–2824PubMedGoogle Scholar
  17. 17.
    Beuchat L (1994) Antimicrobial properties of spices and their essential oils. Nat Antimicrob Syst Food Preserv 12:257–262Google Scholar
  18. 18.
    Lis-Balchin M, Deans S (1997) Bioactivity of selected plant essential oils against Listeria monocytogenes. J Appl Microbiol 82(6):759–762PubMedGoogle Scholar
  19. 19.
    Tajkarimi MM, Ibrahim SA, Cliver DO (2010) Antimicrobial herb and spice compounds in food. Food Control 21(9):1199–1218. Google Scholar
  20. 20.
    Shan B, Cai Y-Z, Brooks JD, Corke H (2007) The in vitro antibacterial activity of dietary spice and medicinal herb extracts. Int J Food Microbiol 117(1):112–119PubMedGoogle Scholar
  21. 21.
    Mahboubi A, Asgarpanah J, Sadaghiyani PN, Faizi M (2015) Total phenolic and flavonoid content and antibacterial activity of Punica granatum L. var. pleniflora flowers (Golnar) against bacterial strains causing foodborne diseases. BMC Complement Altern Med 15:366. PubMedPubMedCentralGoogle Scholar
  22. 22.
    Nakayama M, Shimatani K, Ozawa T, Shigemune N, Tomiyama D, Yui K, Katsuki M, Ikeda K, Nonaka A, Miyamoto T (2015) Mechanism for the antibacterial action of epigallocatechin gallate (EGCg) on Bacillus subtilis. Biosci Biotechnol Biochem 79(5):845–854. PubMedGoogle Scholar
  23. 23.
    Daglia M (2012) Polyphenols as antimicrobial agents. Curr Opin Biotechnol 23(2):174–181. PubMedGoogle Scholar
  24. 24.
    Borges A, Ferreira C, Saavedra MJ, Simoes M (2013) Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic bacteria. Microb Drug Resist 19(4):256–265PubMedGoogle Scholar
  25. 25.
    Yang C-H, Chang H-W, Lin H-Y, Chuang L-Y (2013) Evaluation of antioxidant and antimicrobial activities from 28 Chinese herbal medicines. J Pharmacogn Phytochem 2(1):294–305Google Scholar
  26. 26.
    Do J-R, Kim K-J, Park S-Y, Lee O-H, Kim B-S, Kang S-N (2005) Antimicribial and antioxidant activities of ethanol extracts of medicinal plants. Prev Nutr Food Sci 10(1):81–87Google Scholar
  27. 27.
    Janovska D, Kubikova K, Kokoska L (2003) Screening for antimicrobial activity of some medicinal plants species of traditional Chinese medicine. Czech J Food Sci 21(3):107–110Google Scholar
  28. 28.
    Lee H-A, Hong S, Oh H-G, Park S-H, Kim Y-C, Park H, Jeong G-S, Kim O (2010) Antibacterial activity of Sanguisorba officinalis against Helicobacter pylori. Lab Anim Res 26(3):257–263Google Scholar
  29. 29.
    Feng S, Luo Z, Tao B, Chen C (2015) Ultrasonic-assisted extraction and purification of phenolic compounds from sugarcane (Saccharum officinarum L.) rinds. LWT Food Sci Technol 60(2):970–976Google Scholar
  30. 30.
    Joven J, Espinel E, Rull A, Aragonès G, Rodríguez-Gallego E, Camps J, Micol V, Herranz-López M, Menéndez JA, Borrás I (2012) Plant-derived polyphenols regulate expression of miRNA paralogs miR-103/107 and miR-122 and prevent diet-induced fatty liver disease in hyperlipidemic mice. Biochim Biophys Acta BBA Gen Subj 1820(7):894–899Google Scholar
  31. 31.
    Feng S, Luo Z, Tao B, Chen C (2015) Ultrasonic-assisted extraction and purification of phenolic compounds from sugarcane (Saccharum officinarum L.) rinds. LWT Food Sci Technol 60(2):970–976. Google Scholar
  32. 32.
    Kaur C, Kapoor HC (2002) Anti-oxidant activity and total phenolic content of some Asian vegetables. Int J Food Sci Technol 37(2):153–161Google Scholar
  33. 33.
    Guanlin W, Jinhua T, Dan J (2006) Bacteriostatic action and mechanism of Sophora flavescens Ait on Escherichia coli 01 C84010. Sci Agric Sin 39(5):1018–1024Google Scholar
  34. 34.
    Duffy LL, Osmond-McLeod MJ, Judy J, King T (2018) Investigation into the antibacterial activity of silver, zinc oxide and copper oxide nanoparticles against poultry-relevant isolates of Salmonella and Campylobacter. Food Control 92:293–300Google Scholar
  35. 35.
    Vaquero MR, Serravalle LT, De Nadra MM, De Saad AS (2010) Antioxidant capacity and antibacterial activity of phenolic compounds from argentinean herbs infusions. Food Control 21(5):779–785Google Scholar
  36. 36.
    Peng H, Li W, Li H, Deng Z, Zhang B (2017) Extractable and non-extractable bound phenolic compositions and their antioxidant properties in seed coat and cotyledon of black soybean (Glycine max (L.) merr). J Funct Foods 32:296–312Google Scholar
  37. 37.
    Vinatoru M (2001) An overview of the ultrasonically assisted extraction of bioactive principles from herbs. Ultrason Sonochem 8(3):303–313PubMedGoogle Scholar
  38. 38.
    Wang C, Shi L, Fan L, Ding Y, Zhao S, Liu Y, Ma C (2013) Optimization of extraction and enrichment of phenolics from pomegranate (Punica granatum L.) leaves. Ind Crops Prod 42:587–594Google Scholar
  39. 39.
    Zhao Y, Chen B, Yao S (2007) Separation of 20 (S)-protopanaxdiol type ginsenosides and 20 (S)-protopanaxtriol type ginsenosides with the help of macroporous resin adsorption and microwave assisted desorption. Sep Purif Technol 52(3):533–538Google Scholar
  40. 40.
    Silva E, Pompeu D, Larondelle Y, Rogez H (2007) Optimisation of the adsorption of polyphenols from Inga edulis leaves on macroporous resins using an experimental design methodology. Sep Purif Technol 53(3):274–280Google Scholar
  41. 41.
    Sun A, Sun Q, Liu R (2007) Preparative isolation and purification of flavone compounds from Sophora japonica L. by high-speed counter-current chromatography combined with macroporous resin column separation. J Sep Sci 30(7):1013–1018PubMedGoogle Scholar
  42. 42.
    Lorian V (2005) Antibiotics in laboratory medicine. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  43. 43.
    Luo J, Zhang P, Li S, Shah NP (2016) Antioxidant, antibacterial, and antiproliferative activities of free and bound phenolics from peel and flesh of fuji apple. J Food Sci 81(7):M1735–M1742PubMedGoogle Scholar
  44. 44.
    Weerakkody NS, Caffin N, Turner MS, Dykes GA (2010) In vitro antimicrobial activity of less-utilized spice and herb extracts against selected food-borne bacteria. Food Control 21(10):1408–1414Google Scholar
  45. 45.
    Chen X, Shang F, Meng Y, Li L, Cui Y, Zhang M, Qi K, Xue T (2015) Ethanol extract of Sanguisorba officinalis L. inhibits biofilm formation of methicillin-resistant Staphylococcus aureus in an ica-dependent manner. J Dairy Sci 98(12):8486–8491PubMedGoogle Scholar
  46. 46.
    Helander IM, Alakomi H-L, Latva-Kala K, Mattila-Sandholm T, Pol I, Smid EJ, Gorris LG, von Wright A (1998) Characterization of the action of selected essential oil components on Gram-negative bacteria. J Agric Food Chem 46(9):3590–3595Google Scholar
  47. 47.
    Kalemba D, Kunicka A (2003) Antibacterial and antifungal properties of essential oils. Curr Med Chem 10(10):813–829PubMedGoogle Scholar
  48. 48.
    Biernasiuk A, Wozniak M, Bogucka-Kocka A (2015) Determination of free and bounded phenolic acids in the rhizomes and herb of Sanguisorba officinalis L. Curr Issues Pharm Med Sci 28(4):254–256Google Scholar
  49. 49.
    Tanaka T, Nonaka G, Nishioka I (1984) Tannins and related compounds. XVI. Isolation and characterization of six methyl glucoside gallates and a gallic acid glucoside gallate from Sanguisorba officinalis L. Chem Pharm Bull 32(1):117–121Google Scholar
  50. 50.
    Tanaka T, Nonaka G-I, Nishioka I (1983) 7-O-Galloyl-(+)-catechin and 3-O-galloylprocyanidin B-3 from Sanguisorba officinalis. Phytochemistry 22(11):2575–2578Google Scholar
  51. 51.
    Dorta E, González M, Lobo MG, Sánchez-Moreno C, de Ancos B (2014) Screening of phenolic compounds in by-product extracts from mangoes (Mangifera indica L.) by HPLC-ESI-QTOF-MS and multivariate analysis for use as a food ingredient. Food Res Int 57:51–60Google Scholar
  52. 52.
    He Z, Xia W (2007) Analysis of phenolic compounds in Chinese olive (Canarium album L.) fruit by RPHPLC–DAD–ESI–MS. Food Chemistry 105(3):1307–1311Google Scholar
  53. 53.
    Ghareeb MA, Mohamed T, Saad AM, Refahy LAG, Sobeh M, Wink M (2018) HPLC–DAD–ESI–MS/MS analysis of fruits from Firmiana simplex (L.) and evaluation of their antioxidant and antigenotoxic properties. J Pharm Pharmacol 70(1):133–142PubMedGoogle Scholar
  54. 54.
    Abu-Reidah IM, Ali-Shtayeh MS, Jamous RM, Arráez-Román D, Segura-Carretero A (2015) HPLC–DAD–ESI–MS/MS screening of bioactive components from Rhus coriaria L. (Sumac) fruits. Food Chem 166:179–191PubMedGoogle Scholar
  55. 55.
    Santos SA, Villaverde JJ, Freire CS, Domingues MRM, Neto CP, Silvestre AJ (2012) Phenolic composition and antioxidant activity of Eucalyptus grandis, E. urograndis (E. grandis × E. urophylla) and E. maidenii bark extracts. Ind Crops Prod 39:120–127Google Scholar
  56. 56.
    Lee J-H, Johnson JV, Talcott ST (2005) Identification of ellagic acid conjugates and other polyphenolics in muscadine grapes by HPLC–ESI–MS. J Agric Food Chem 53(15):6003–6010PubMedGoogle Scholar
  57. 57.
    Bakr RO, Wasfi R, Swilam N, Sallam IE (2016) Characterization of the bioactive constituents of Nymphaea alba rhizomes and evaluation of anti-biofilm as well as antioxidant and cytotoxic properties. J Med Plants Res 10(26):390–401Google Scholar
  58. 58.
    Fernandes A, Sousa A, Mateus N, Cabral M, de Freitas V (2011) Analysis of phenolic compounds in cork from Quercus suber L. by HPLC–DAD/ESI–MS. Food Chem 125(4):1398–1405Google Scholar
  59. 59.
    Jia X, Luo H, Xu M, Zhai M, Guo Z, Qiao Y, Wang L (2018) Dynamic changes in phenolics and antioxidant capacity during Pecan (Carya illinoinensis) kernel ripening and its phenolics profiles. Molecules 23(2):435PubMedCentralGoogle Scholar
  60. 60.
    Teegarden MD, Schwartz SJ, Cooperstone JL (2019) Profiling the impact of thermal processing on black raspberry phytochemicals using untargeted metabolomics. Food Chem 274:782–788PubMedGoogle Scholar
  61. 61.
    G-i Nonaka, Tanaka T, Nishioka I (1982) Tannins and related compounds. Part 3. A new phenolic acid, sanguisorbic acid dilactone, and three new ellagitannins, sanguiins H-1, H-2, and H-3, from Sanguisorba officinalis. J Chem Soc Perkin Trans 1:1067–1073Google Scholar
  62. 62.
    García-Villalba R, Espín JC, Aaby K, Alasalvar C, Heinonen M, Jacobs G, Voorspoels S, Koivumäki T, Kroon PA, Pelvan E (2015) Validated method for the characterization and quantification of extractable and nonextractable ellagitannins after acid hydrolysis in pomegranate fruits, juices, and extracts. J Agric Food Chem 63(29):6555–6566PubMedGoogle Scholar
  63. 63.
    Santos SA, Villaverde JJ, Sousa AF, Coelho JF, Neto CP, Silvestre AJ (2013) Phenolic composition and antioxidant activity of industrial cork by-products. Ind Crops Prod 47:262–269Google Scholar
  64. 64.
    Fischer UA, Carle R, Kammerer DR (2011) 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 127(2):807–821PubMedGoogle Scholar
  65. 65.
    Baczek K (2014) Accumulation of biomass and phenolic compounds in Polish and Mongolian great burnet (Sanguisorba officinalis L.) populations. Herba Pol 60(3):44–55Google Scholar
  66. 66.
    Zhang S, Liu X, Zhang Z-L, He L, Wang Z, Wang G-S (2012) Isolation and identification of the phenolic compounds from the roots of Sanguisorba officinalis L. and their antioxidant activities. Molecules 17(12):13917–13922PubMedPubMedCentralGoogle Scholar
  67. 67.
    Zhao Y, Chen P, Lin L, Harnly J, Yu LL, Li Z (2011) Tentative identification, quantitation, and principal component analysis of green pu-erh, green, and white teas using UPLC/DAD/MS. Food Chem 126(3):1269–1277PubMedPubMedCentralGoogle Scholar
  68. 68.
    Vallverdú-Queralt A, Boix N, Piqué E, Gómez-Catalan J, Medina-Remon A, Sasot G, Mercader-Martí M, Llobet JM, Lamuela-Raventos RM (2015) Identification of phenolic compounds in red wine extract samples and zebrafish embryos by HPLC–ESI–LTQ–Orbitrap–MS. Food Chem 181:146–151PubMedGoogle Scholar
  69. 69.
    Biswas D, Roymon M (2013) LC/TOF/ESI/MS based detection of bioactive compounds present in leaf and bark extract of Acacia arabica. Recent Res Sci Technol 5(2):37–40Google Scholar
  70. 70.
    Ma J, Yang H, Basile MJ, Kennelly EJ (2004) Analysis of polyphenolic antioxidants from the fruits of three Pouteria species by selected ion monitoring liquid chromatography–mass spectrometry. J Agric Food Chem 52(19):5873–5878PubMedGoogle Scholar
  71. 71.
    Sha M, Cao A, Wang B, Liu C, Geng J, Liu W (1998) Determination of hyperin in Sanguisorba officinalis L. by high performance liquid chromatography. Se pu Chin J Chromatogr 16(3):226–228Google Scholar
  72. 72.
    Ma Z, Zheng S, Han H, Meng J, Yang X, Zeng S, Zhou H, Jiang H (2016) The bioactive components of Coreopsis tinctoria (Asteraceae) capitula: antioxidant activity in vitro and profile in rat plasma. J Funct Foods 20:575–586Google Scholar
  73. 73.
    Tao W, Yang N, Duan Ja WuD, Guo J, Tang Y, Qian D, Zhu Z (2011) Simultaneous determination of eleven major flavonoids in the pollen of Typha angustifolia by HPLC–PDA–MS. Phytochem Anal 22(5):455–461PubMedGoogle Scholar
  74. 74.
    Nakamura T, Kinjo C, Nakamura Y, Kato Y, Nishikawa M, Hamada M, Nakajima N, Ikushiro S, Murota K (2018) Lymphatic metabolites of quercetin after intestinal administration of quercetin-3-glucoside and its aglycone in rats. Arch Biochem Biophys 645:126–136PubMedGoogle Scholar
  75. 75.
    Du XG, Wang W, Zhang QY, Cheng J, Avula B, Khan IA, Guo DA (2012) Identification of xanthones from Swertia punicea using high-performance liquid chromatography coupled with electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 26(24):2913–2923PubMedGoogle Scholar
  76. 76.
    Chen L-J, Games DE, Jones J (2003) Isolation and identification of four flavonoid constituents from the seeds of Oroxylum indicum by high-speed counter-current chromatography. J Chromatogr A 988(1):95–105PubMedGoogle Scholar
  77. 77.
    Daglia M (2012) Polyphenols as antimicrobial agents. Curr Opin Biotechnol 23(2):174–181PubMedGoogle Scholar
  78. 78.
    Pinho E, Ferreira IC, Barros L, Carvalho AM, Soares G, Henriques M (2014) Antibacterial potential of northeastern Portugal wild plant extracts and respective phenolic compounds. BioMed Res Int 2014:1–8Google Scholar
  79. 79.
    Vaquero MR, Alberto MR, De Nadra MM (2007) Antibacterial effect of phenolic compounds from different wines. Food Control 18(2):93–101Google Scholar
  80. 80.
    Quave CL, Estévez-Carmona M, Compadre CM, Hobby G, Hendrickson H, Beenken KE, Smeltzer MS (2012) Ellagic acid derivatives from Rubus ulmifolius inhibit Staphylococcus aureus biofilm formation and improve response to antibiotics. PLoS One 7(1):e28737PubMedPubMedCentralGoogle Scholar
  81. 81.
    Bhattacharya D, Ghosh D, Bhattacharya S, Sarkar S, Karmakar P, Koley H, Gachhui R (2018) Antibacterial activity of polyphenolic fraction of Kombucha against Vibrio cholerae: targeting cell membrane. Lett Appl Microbiol 66(2):145–152PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Hong-lin Zhu
    • 1
  • Gang Chen
    • 1
    Email author
  • Sun-ni Chen
    • 1
  • Qi-rui Wang
    • 1
  • Ling Wan
    • 1
  • Su-ping Jian
    • 1
  1. 1.State Key Laboratory of Food Science and TechnologyNanchang UniversityNanchangChina

Personalised recommendations