Advertisement

Exploring the powerful phytoarsenal of white grape marc against bacteria and parasites causing significant diseases

Abstract

Natural extracts containing high polyphenolic concentration possess antibacterial, anti-parasitic and fungicidal activities. The present research characterises two extracts based on white grape marc, a winemaking by-product, describing their physicochemical features and antimicrobial capacities. The main components of these extracts are phenolic acids, flavan-3-ols and their gallates and flavonols and their glycosides. As a result of this complex composition, the extracts showed pronounced bioactivities with potential uses in agricultural, pharmaceutical and cosmetic industries. Polyphenol compounds were extracted by using hydro-organic solvent mixtures from the by-product of Albariño white wines (Galicia, NW Spain) production. The in vitro antimicrobial activity of these extracts was evaluated on Gram-positive and Gram-negative bacteria and Apicomplexan and Oomycota parasites. Microbial species investigated are causing agents of several human and animal diseases, such as foodborne illnesses (Bacillus cereus, Escherichia coli, Salmonella enterica, and Toxoplasma gondii), skin infections and/or mastitis (Staphylococcus aureus and Streptococcus uberis), malaria (Plasmodium falciparum) and plant infections as “chestnut ink” or “root rot” (Phytophthora cinnamomi). Both extracts showed activity against all the tested species, being nontoxic for the host. So, they could be used for the development of biocides to control a wide range of pathogenic agents and contribute to the enhancement of winemaking industry by-products.

This is a preview of subscription content, log in to check access.

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2

References

  1. AAT Bioquest I (2019) Quest graph™ IC50 calculator

  2. Adia MM, Emami SN, Byamukama R, Faye I, Borg-Karlson AK (2016) Antiplasmodial activity and phytochemical analysis of extracts from selected Ugandan medicinal plants. J Ethnopharmacol 186:14–19. https://doi.org/10.1016/J.JEP.2016.03.047

  3. Álvarez-Casas M, García-Jares C, Llompart M, Lores M (2014) Effect of experimental parameters in the pressurized solvent extraction of polyphenolic compounds from white grape marc. Food Chem 157:524–532. https://doi.org/10.1016/j.foodchem.2014.02.078

  4. Anastasiadi M, Chorianopoulos NG, Nychas GJE, Karoutounian SA (2009) Antilisterial activities of polyphenol-rich extracts of grapes and vinification byproducts. J Agric Food Chem 57:457–463. https://doi.org/10.1021/jf8024979

  5. Arima H, Ashida H, Danno G (2002) Rutin-enhanced antibacterial activities of flavonoids against Bacillus cereus and Salmonella enteritidis. Biosci Biotechnol Biochem 66:1009–1014. https://doi.org/10.1271/bbb.66.1009

  6. Arima H, Danno G (2002) Isolation of antimicrobial compounds from guava (Psidium guajava L.) and their structural elucidation. Biosci Biotechnol Biochem 66:1727–1730. https://doi.org/10.1271/bbb.66.1727

  7. Azami SJ, Amani A, Keshavarz H, Najafi-Taher R, Mohebali M, Faramarzi MA, Mahmoudi M, Shojaee S (2018) Nanoemulsion of atovaquone as a promising approach for treatment of acute and chronic toxoplasmosis. Eur J Pharm Sci 117:138–146. https://doi.org/10.1016/j.ejps.2018.02.018

  8. El Babili F, Bouajila J, Souchard JP et al (2011) Oregano: chemical analysis and evaluation of its antimalarial, antioxidant, and cytotoxic activities. J Food Sci 76:512–518. https://doi.org/10.1111/j.1750-3841.2011.02109.x

  9. Bargiacchi E, Campo M, Romani A et al (2017) Hydrolysable tannins from sweet chestnut (Castanea sativa Mill.) to improve tobacco and food/feed quality. Note 1: fraction characterization, and tobacco biostimulant effect for gall-nematode resistance. AIMS Agric Food 2:324–338. https://doi.org/10.3934/agrfood.2017.3.324

  10. Benabderrahmane W, Amrani A, Benaissa O et al (2018) Chemical constituents, in vitro antioxidant and antimicrobial properties of ethyl acetate extract obtained from Cytisus triflorus l'Her. Nat Prod Res 22:1–5. https://doi.org/10.1080/14786419.2018.1519816

  11. Benabderrahmane W, Lores M, Benaissa O et al (2019) Polyphenolic content and bioactivities of Crataegus oxyacantha L (Rosaceae). Nat Prod Res 5:1–6. https://doi.org/10.1080/14786419.2019.1582044

  12. Beres C, Costa GNS, Cabezudo I, da Silva-James NK, Teles ASC, Cruz APG, Mellinger-Silva C, Tonon RV, Cabral LMC, Freitas SP (2017) Towards integral utilization of grape pomace from winemaking process: a review. Waste Manag 68:581–594. https://doi.org/10.1016/J.WASMAN.2017.07.017

  13. Borges A, Ferreira C, Saavedra MJ, Simões M (2013) Antibacterial activity and mode of action of ferulic and gallic acids against pathogenic Bacteria. Microb Drug Resist 19:256–265. https://doi.org/10.1089/mdr.2012.0244

  14. Borrmann S, Szlezák N, Faucher J et al (2002) Artesunate and praziquantel for the treatment of Schistosoma haematobium infections: a double-blind, randomized, placebo-controlled study. J Infect Dis 184:1363–1366. https://doi.org/10.1086/324004

  15. Bottari NB, Baldissera MD, Tonin AA, Rech VC, Nishihira VS, Thomé GR, Camillo G, Vogel FF, Duarte MM, Schetinger MR, Morsch VM, Tochetto C, Fighera R, da Silva AS (2015) Effects of sulfamethoxazole-trimethoprim associated to resveratrol on its free form and complexed with 2-hydroxypropyl-β-cyclodextrin on cytokines levels of mice infected by toxoplasma gondii. Microb Pathog 87:40–44. https://doi.org/10.1016/j.micpath.2015.07.013

  16. Budiman I, Tjokropranoto R, Widowati W et al (2014) Antioxidant and anti-malarial properties of catechins. Br J Med Med Res 5:895–902. https://doi.org/10.9734/bjmmr/2015/11451

  17. Chauhan K, Kaur G, Kaur S (2018) Activity of rutin, a potent flavonoid against SSG-sensitive and -resistant Leishmania donovani parasites in experimental leishmaniasis. Int Immunopharmacol 64:372–385. https://doi.org/10.1016/J.INTIMP.2018.09.026

  18. Chiva-Blanch G, Urpi-Sarda M, Llorach R, Rotches-Ribalta M, Guillén M, Casas R, Arranz S, Valderas-Martinez P, Portoles O, Corella D, Tinahones F, Lamuela-Raventos RM, Andres-Lacueva C, Estruch R (2012) Differential effects of polyphenols and alcohol of red wine on the expression of adhesion molecules and inflammatory cytokines related to atherosclerosis: a randomized clinical trial. Am J Clin Nutr 95:326–334. https://doi.org/10.3945/ajcn.111.022889

  19. Corrales M, Han JH, Tauscher B (2009) Antimicrobial properties of grape seed extracts and their effectiveness after incorporation into pea starch films. Int J Food Sci Technol 44:425–433. https://doi.org/10.1111/j.1365-2621.2008.01790.x

  20. Davison EM (2002) Book Review. Plant Pathol 51:255–255. https://doi.org/10.1046/j.0032-0862.2002.00668_6.x

  21. de O Ribeiro IC, Mariano EGA, Careli RT, Morais-Costa F, de Sant'Anna FM, Pinto MS, de Souza MR, Duarte ER (2018) Plants of the Cerrado with antimicrobial effects against Staphylococcus spp. and Escherichia coli from cattle. BMC Vet Res 14:32. https://doi.org/10.1186/s12917-018-1351-1

  22. Deng Q, Zhao Y (2011) Physicochemical, nutritional, and antimicrobial properties of wine grape (cv. Merlot) pomace extract-based films. J Food Sci 76:309–317. https://doi.org/10.1111/j.1750-3841.2011.02090.x

  23. Dohutia C, Chetia D, Gogoi K, Sarma K (2017) Design, in silico and in vitro evaluation of curcumin analogues against Plasmodium falciparum. Exp Parasitol 175:51–58. https://doi.org/10.1016/j.exppara.2017.02.006

  24. Ekanem AP, Brisibe EA (2010) Effects of ethanol extract of Artemisia annua L. against monogenean parasites of Heterobranchus longifilis. Parasitol Res 106:1135–1139. https://doi.org/10.1007/s00436-010-1787-0

  25. European Centre for Disease Prevention and Control (ECDC), European Food Safety Authority, European Medicines Agency (2017) Second joint interagency antimicrobial consumption and resistance analysis (JIACRA) report. John Wiley & Sons, Ltd

  26. European Food Safety Authority (EFSA) (2019) Monitoring and analysis of food-borne diseases. http://www.efsa.europa.eu/en/topics/topic/monitoring-foodborne-diseases. Accessed 29 Apr 2019

  27. Castillo-Reyes F, Hernandez-Castillo FD, Clemente-Constantino JA et al (2015) In vitro antifungal activity of polyphenols-rich plant extracts against Phytophthora cinnamomi Rands. African J Agric Res 10:4554–4560. https://doi.org/10.5897/ajar2013.8072

  28. Friedman M (2014) Antibacterial, antiviral, and antifungal properties of wines and winery byproducts in relation to their flavonoid content. J Agric Food Chem 62:6025–6042. https://doi.org/10.1021/jf501266s

  29. Ganesh D, Fuehrer HP, Starzengrüber P, Swoboda P, Khan WA, Reismann JA, Mueller MS, Chiba P, Noedl H (2012) Antiplasmodial activity of flavonol quercetin and its analogues in Plasmodium falciparum: evidence from clinical isolates in Bangladesh and standardized parasite clones. Parasitol Res 110:2289–2295. https://doi.org/10.1007/s00436-011-2763-z

  30. García-Pineda E, Benezer-Benezer M, Gutiérrez-Segundo A, Rangel-Sánchez G, Arreola-Cortés A, Castro-Mercado E (2010) Regulation of defence responses in avocado roots infected with Phytophthora cinnamomi (Rands). Plant Soil 331:45–56. https://doi.org/10.1007/s11104-009-0225-5

  31. González-Centeno MR, Jourdes M, Femenia A, Simal S, Rosselló C, Teissedre PL (2013) Characterization of polyphenols and antioxidant potential of white grape pomace byproducts (Vitis vinifera L.). J Agric Food Chem 61:11579–11587. https://doi.org/10.1021/jf403168k

  32. Grellier P, Nemeikaite-Čeniene A, Šarlauskas J, Čenas N (2008) Role of single-electron oxidation potential and lipophilicity in the antiplasmodial in vitro activity of polyphenols: comparison to mammalian cells. Zeitschrift fur Naturforsch - Sect C J Biosci 63:445–450. https://doi.org/10.1515/znc-2008-5-622

  33. Guerra-Rivas C, Gallardo B, Mantecón ÁR, del Álamo-Sanza M, Manso T (2017) Evaluation of grape pomace from red wine by-product as feed for sheep. J Sci Food Agric 97:1885–1893. https://doi.org/10.1002/jsfa.7991

  34. Gutteridge JMC, Halliwell B (2010) Antioxidants: molecules, medicines, and myths. Biochem Biophys Res Commun 393:561–564. https://doi.org/10.1016/J.BBRC.2010.02.071

  35. Ietta F, Maioli E, Daveri E, Gonzaga Oliveira J, da Silva RJ, Romagnoli R, Cresti L, Maria Avanzati A, Paulesu L, Barbosa BF, Gomes AO, Roberto Mineo J, Ferro EAV (2017) Rottlerin-mediated inhibition of toxoplasma gondii growth in BeWo trophoblast-like cells. Sci Rep 7:1279. https://doi.org/10.1038/s41598-017-01525-6

  36. Judelson HS, Blanco FA (2005) The spores of Phytophthora: weapons of the plant destroyer. Nat Rev Microbiol 3:47–58

  37. Julianti T, De Mieri M, Zimmermann S et al (2014) HPLC-based activity profiling for antiplasmodial compounds in the traditional Indonesian medicinal plant Carica papaya L. J Ethnopharmacol 155:426–434. https://doi.org/10.1016/j.jep.2014.05.050

  38. Kajiya K, Hojo H, Suzuki M, Nanjo F, Kumazawa S, Nakayama T (2004) Relationship between antibacterial activity of (+)-catechin derivatives and their interaction with a model membrane. J Agric Food Chem 52:1514–1519. https://doi.org/10.1021/jf0350111

  39. Khasanah U, WidyaWaruyanti A, Hafid A, Tanjung M (2017) Antiplasmodial activity of isolated polyphenols from Alectryon serratus leaves against 3D7 Plasmodium falciparum. Pharm Res 9:57. https://doi.org/10.4103/pr.pr_39_17

  40. Kim WS, Choi WJ, Lee S, Kim WJ, Lee DC, Sohn UD, Shin HS, Kim W (2015) Anti-inflammatory, antioxidant and antimicrobial effects of artemisinin extracts from Artemisia annua L. Korean J Physiol Pharmacol 19:21–27. https://doi.org/10.4196/kjpp.2015.19.1.21

  41. Lores M, García-Jares C, Álvarez-Casas M, Llompart M (2014a) Extracto polifenólico a partir de residuos de uva blanca. ES 2 443 547

  42. Lores M,García-Jares C, Álvarez-Casas M, Llompart M (2014b) Polyphenolic extract from white grape residue. WO 2014/013122 A1

  43. Mattos GN, Tonon RV, Furtado AAL, Cabral LM (2017) Grape by-product extracts against microbial proliferation and lipid oxidation: a review. J Sci Food Agric 97:1055–1064

  44. Mendoza L, Cotoras M, Vivanco M et al (2013) Evaluation of antifungal properties against the phytopathogenic fungus botrytis cinerea of anthocyanin rich-extracts obtained from grape pomaces. J Chil Chem Soc 58:1725–1727. https://doi.org/10.4067/S0717-97072013000200018

  45. Miklasińska M, Kȩpa M, Wojtyczka RD et al (2016) Catechin hydrate augments the antibacterial action of selected antibiotics against Staphylococcus aureus clinical strains. Molecules 21:244. https://doi.org/10.3390/molecules21020244

  46. Moon HI, Sim J (2008) Antimalarial activity in mice of resveratrol derivative from Pleuropterus ciliinervis. Ann Trop Med Parasitol 102:447–450. https://doi.org/10.1179/136485908x300832

  47. Murphy D, Ricci A, Auce Z et al (2017) EMA and EFSA joint scientific opinion on measures to reduce the need to use antimicrobial agents in animal husbandry in the European Union, and the resulting impacts on food safety (RONAFA). EFSA J 15. https://doi.org/10.2903/j.efsa.2017.4666

  48. Piscopo M, Tenore GC, Notariale R, Maresca V, Maisto M, de Ruberto F, Heydari M, Sorbo S, Basile A (2019) Antimicrobial and antioxidant activity of proteins from Feijoa sellowiana berg. Fruit before and after in vitro gastrointestinal digestion. Nat Prod Res 2019(2):1–5. https://doi.org/10.1080/14786419.2018.1543686

  49. Placha I, Chrastinova L, Laukova A, Cobanova K, Takacova J, Strompfova V, Chrenkova M, Formelova Z, Faix S (2013) Effect of thyme oil on small intestine integrity and antioxidant status, phagocytic activity and gastrointestinal microbiota in rabbits. Acta Vet Hung 61:197–208. https://doi.org/10.1556/AVet.2013.012

  50. Sagdic O, Ozturk I, Ozkan G, Yetim H, Ekici L, Yilmaz MT (2011a) RP-HPLC–DAD analysis of phenolic compounds in pomace extracts from five grape cultivars: evaluation of their antioxidant, antiradical and antifungal activities in orange and apple juices. Food Chem 126:1749–1758. https://doi.org/10.1016/j.foodchem.2010.12.075

  51. Sagdic O, Ozturk I, Yilmaz MT, Yetim H (2011b) Effect of grape pomace extracts obtained from different grape varieties on microbial quality of beef Patty. J Food Sci 76:M515–M521. https://doi.org/10.1111/j.1750-3841.2011.02323.x

  52. Seeber F, Steinfelder S (2016) Recent advances in understanding apicomplexan parasites. F1000Research 5:1369. https://doi.org/10.12688/f1000research.7924.1

  53. Serra AT, Matias AA, Nunes AVM et al (2008) In vitro evaluation of olive- and grape-based natural extracts as potential preservatives for food. Innov Food Sci Emerg Technol 9:311–319. https://doi.org/10.1016/j.ifset.2007.07.011

  54. Silveira P, Vashist U, Cabral A, Amaral KB, Soares GL, Dagosto M (2009) Effect of rutin and chloroquine on white Leghorn chickens infected with Plasmodium (Bennettinia) juxtanucleare. Trop Anim Health Prod 41:1319–1323. https://doi.org/10.1007/s11250-009-9317-8

  55. Simões M, Bennett RN, Rosa EAS (2009) Understanding antimicrobial activities of phytochemicals against multidrug resistant bacteria and biofilms. Nat Prod Rep 26:746–757

  56. Slavic K, Derbyshire ET, Naftalin RJ, Krishna S, Staines HM (2009) Comparison of effects of green tea catechins on apicomplexan hexose transporters and mammalian orthologues. Mol Biochem Parasitol 168:113–116. https://doi.org/10.1016/j.molbiopara.2009.06.008

  57. Smilkstein M, Sriwilaijaroen N, Kelly JX, Wilairat P, Riscoe M (2004) Simple and inexpensive fluorescence-based technique for high-throughput antimalarial drug screening. Antimicrob Agents Chemother 48:1803–1806. https://doi.org/10.1128/AAC.48.5.1803-1806.2004

  58. Somsak V, Damkaew A, Onrak P (2018) Antimalarial activity of Kaempferol and its combination with Chloroquine in Plasmodium berghei infection in mice. J Pathog 2018:1–7. https://doi.org/10.1155/2018/3912090

  59. Tauxe RV, Doyle MP, Kuchenmüller T, Schlundt J, Stein CE (2010) Evolving public health approaches to the global challenge of foodborne infections. Int J Food Microbiol 139:S16–S28. https://doi.org/10.1016/j.ijfoodmicro.2009.10.014

  60. Tayengwa T, Mapiye C (2018) Citrus and winery wastes: promising dietary supplements for sustainable ruminant animal nutrition, health, production, and meat quality. Sustain. 10:3718

  61. Taylor RL (1950) American association for the advancement of science. J Clin Endocrinol Metab 10:1361–1362. https://doi.org/10.1210/jcem-10-10-1361

  62. Tenore GC, Basile A, Novellino E (2011) Antioxidant and antimicrobial properties of polyphenolic fractions from selected Moroccan red wines. J Food Sci 76:C1342–C1348. https://doi.org/10.1111/j.1750-3841.2011.02426.x

  63. Tortora F, Notariale R, Maresca V, Good KV, Sorbo S, Basile A, Manna C (2019) Phenol-rich Feijoa sellowiana (pineapple guava) extracts protect human red blood cells from mercury-induced cellular toxicity. Antioxidants 8:220. https://doi.org/10.3390/antiox8070220

  64. Veluri R, Weir TL, Bais HP, Stermitz FR, Vivanco JM (2004) Phytotoxic and antimicrobial activities of catechin derivatives. J Agric Food Chem 52:1077–1082. https://doi.org/10.1021/jf030653+

  65. World Health Organization Malaria (2019) In: Malaria. https://www.who.int/news-room/fact-sheets/detail/malaria. Accessed 29 Apr 2019

  66. Yadav D, Kumar A, Kumar P, Mishra D (2015) Antimicrobial properties of black grape (Vitis vinifera L.) peel extracts against antibiotic-resistant pathogenic bacteria and toxin producing molds. Indian J Pharmacol 47:663. https://doi.org/10.4103/0253-7613.169591

  67. Yammine S, Brianceau S, Manteau S, Turk M, Ghidossi R, Vorobiev E, Mietton-Peuchot M (2018) Extraction and purification of high added value compounds from by-products of the winemaking chain using alternative/nonconventional processes/technologies. Crit Rev Food Sci Nutr 58:1375–1390. https://doi.org/10.1080/10408398.2016.1259982

  68. Yan C, Liang LJ, Zheng KY, Zhu XQ (2016) Impact of environmental factors on the emergence, transmission and distribution of toxoplasma gondii. Parasites and Vectors 9:137

  69. Zampelas A, Micha R (2015) Antioxidants in health and disease. BMJ Publishing Group

Download references

Acknowledgements

This research was supported by projects GPC2017/04 (Consolidated Research Groups Program) & ED431E 2018/01 Cross-Research in Environmental Technologies (CRETUS) (Xunta de Galicia, Spain).

Author information

Correspondence to Trinidad de Miguel.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible editor: Giovanni Benelli

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Rama, J.R., Mallo, N., Biddau, M. et al. Exploring the powerful phytoarsenal of white grape marc against bacteria and parasites causing significant diseases. Environ Sci Pollut Res (2020) doi:10.1007/s11356-019-07472-1

Download citation

Keywords

  • Antibacterial
  • Anti-parasitic
  • Enhancement of winemaking by-products
  • Grape marc
  • Natural extract
  • Polyphenols