Sulforaphane-enriched extracts from glucoraphanin-rich broccoli exert antimicrobial activity against gut pathogens in vitro and innovative cooking methods increase in vivo intestinal delivery of sulforaphane

Salah Abukhabta,Cheryl Latimer,Roger Lawther,Sameer Khalil Ghawi,L Kirsty Pourshahidi,Gordon Mcdougall,J Will Allwood,Siobhan Lavery,Ian Rowland,Chris I R Gill,Gloria O’Connor,Dimitris Charalampopoulos,Kimon Andreas Karatzas,Susan Verrall

doi:10.1007/s00394-020-02322-0

Abstract

PurposeStudies on broccoli (Brassica oleracea var. italica) indicate beneficial effects against a range of chronic diseases, commonly attributed to their bioactive phytochemicals. Sulforaphane, the bioactive form of glucoraphanin, is formed by the action of the indigenous enzyme myrosinase. This study explored the role that digestion and cooking practices play in bioactivity and bioavailability, especially the rarely considered dose delivered to the colon.MethodsThe antimicrobial activity of sulforaphane extracts from raw, cooked broccoli and cooked broccoli plus mustard seeds (as a source myrosinase) was assessed. The persistence of broccoli phytochemicals in the upper gastrointestinal tract was analysed in the ileal fluid of 11 ileostomates fed, in a cross-over design, broccoli soup prepared with and without mustard seeds.ResultsThe raw broccoli had no antimicrobial activity, except against Bacillus cereus, but cooked broccoli (with and without mustard seeds) showed considerable antimicrobial activity against various tested pathogens. The recovery of sulforaphane in ileal fluids post soup consumption was < 1% but the addition of mustard seeds increased colon-available sulforaphane sixfold. However, when sulforaphane was extracted from the ileal fluid with the highest sulforaphane content and tested against Escherichia coli K12, no inhibitory effects were observed. Analysis of glucosinolates composition in ileal fluids revealed noticeable inter-individual differences, with six “responding” participants showing increases in glucosinolates after broccoli soup consumption.ConclusionsSulforaphane-rich broccoli extracts caused potent antimicrobial effects in vitro, and the consumption of sulforaphane-enriched broccoli soup may inhibit bacterial growth in the stomach and upper small intestine, but not in the terminal ileum or the colon.

Highlights

Broccoli (Brassica oleracea var. italica) is a member of the Brassicaceae family of plants
Sulforaphane nitrile level increased after the addition of mustard seeds (0.05 vs 0.69 μmol/g DW), this increase is low compared to the level formed in broccoli before cooking (0.69 vs 9.9 μmol/g DW)
This study explored the role that digestion and cooking practices play in bioactivity and bioavailability, especially the rarely considered dose delivered to the colon

Summary

Introduction

Broccoli (Brassica oleracea var. italica) is a member of the Brassicaceae family of plants. The beneficial effects are commonly attributed to bioactive phytochemicals present that includes hydroxycinnamic acids, flavonoids (e.g., quercetin, kaempferol, myricetin), carotenoids (lutein) and glucosinolates (e.g., glucoraphanin) [8,9,10]. The biologically active forms of the glucosinolates are isothiocyanates which are generated by the action of the enzyme myrosinase that is released when the plant tissue is chopped or chewed [12]. In the case of glucoraphanin, the isothiocyanate formed is sulforaphane, less bioactive nitriles can be formed by the activity of epithiospecifier protein (ESP) [13]. Sulforaphane has been shown in vitro to exert bioactivity [14,15,16,17,18] and to exert antibacterial effects against a range of food-borne pathogens and enteropathogenic microbes including Listeria monocytogenes, Escherichia coli, Salmonella Typhimurium and Helicobacter pylori [9, 19,20,21]

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