Abstract
The effects of sumac, cumin, black pepper and red pepper diethyl ether extracts on the growth of eight foodborne pathogens (FBP) and their biogenic amine (BA) production were investigated in histidine decarboxylase broth. The antimicrobial effect was determined by the minimum inhibitory (MIC) and minimum bactericidal (MBC) concentrations. Sumac extract showed the highest antimicrobial activity against FBP. Enterococcus faecalis and Aeromonas hydrophila were the most susceptible strains to sumac extract. The MBC of spice extracts on the FBP was generally above 50 mg/mL. Cumin extract was the most effective in decreasing bacterial loads, inhibiting significantly the microbial growth of Staphylococcus aureus, Pseudomonas aeruginosa, Campylobacter jejuni and A. hydrophila. Histamine production ranged from 0.14 (Yersinia enterocolitica) to 39.29 mg/L (S. aureus). Cumin extract significantly inhibited the histamine formation by S. aureus and Salmonella paratyphi A. Black and red pepper extracts promoted the histamine formation by most of FBP under scrutiny. Red pepper extract generally increased formation of BA, while sumac and cumin extracts proved to be the most effective antimicrobials and BA formation inhibitors. This research study allowed to conclude that sumac and cumin extracts can be used as natural preservatives in the agro-food industry.
Similar content being viewed by others
References
Schirone M, Visciano P (2021) Trends of major foodborne outbreaks in the european union during the years 2015–2019. Hyg 1:106–119
Pijnacker R, Friesema IHM, Mughini Gras L, Lagerweij GR, Van Pelt W, Franz E (2019) Disease burden of food-related pathogens in the Netherlands, 2018. National Institute for Public Health and the Environment, Netherlands
Pires SM, Desta BN, Mughini-Gras L, Mmbaga BT, Fayemi OE, Salvador EM, Gobena T, Majowicz SE, Hald T, Hoecskov PS, Yukiminato S, Devleesschauwer B (2021) Burden of foodborne diseases: Think global, act local. Curr Op Food Sci 39:152–159
Özogul Y, Özogul F (2020). In: Saad B, Tofalo R (eds) Biogenic amines in food: analysis, occurrence and toxicity. The Royal Society of Chemistry, London
EFSA (2011) EFSA panel on biological hazards scientific opinion on risk based control of biogenic amine formation in fermented foods. EFSA Journal 9:23
Ladero V, Calles-Enriquez M, Fernandez MA, Alvarez M (2010) Toxicological effects of dietary biogenic amines. Curr Nutr Food Sci 6:145–156
del Rio B, Redruello B, Linares DM, Ladero V, Fernandez M, Martin MC, Ruas-Madiedo P, Alvarez MA (2017) The dietary biogenic amines tyramine and histamine show synergistic toxicity towards intestinal cells in culture. Food Chem 218:249–255
Don LZ (1997) The impact of consumer demands and trends on food processing. Emerg Infect Dis 3:467
Tajkarimi MM, Ibrahim SA, Cliver DO (2010) Antimicrobial herb and spice compounds in food. Food Control 21:1199–1218
Reverter M, Bontemps N, Lecchini D, Banaigs B, Sasal P (2014) Use of plant extracts in fish aquaculture as an alternative to chemotherapy: current status and future perspectives. Aquaculture 433:50–61
Roby MHH, Sarhan MA, Selim KAH, Khalel KI (2013) Evaluation of antioxidant activity, total phenols and phenolic compounds in thyme (Thymus vulgaris L.), sage (Salvia officinalis L.), and marjoram (Origanum majorana L.) extracts. Indust Crop Prod 43:827–831
Wetherilt H, Pala M (1994) Herbs and spices indigenous to Turkey. Elsevier Science, BV Amsterdam
Ahmad N, Fazal H, Abbasi BH, Farooq S, Ali M, Khan MA (2012) Biological role of Piper nigrum L. (Black pepper). Asian Pac J Trop Biomed 2:S1945–S1953
Koffi-Nevry R, Kouassi KC, Nanga ZY, Koussémon M, Loukou GY (2012) Antibacterial activity of two bell pepper extracts: Capsicum annuum L. and Capsicum frutescens. Int J Food Prop 15:961–971
Rayne S, Mazza G (2007) Biological activities of extracts from sumac (Rhus spp.). Plant Foods Hum Nutr 62:165–175
Sowbhagya HB (2013) Chemistry, technology, and nutraceutical functions of cumin (Cuminum cyminum L). Crit Rev Food Sci Nutr 53:1–10
Suhaj M (2006) Spice antioxidants isolation and their antiradical activity. J Food Comp Anal 19:531–537
Mah JH, Kim YJ, Hwang HJ (2009) Inhibitory effects of garlic and other spices on biogenic amine production in Myeolchi-jeot, Korean salted and fermented anchovy product. Food Control 20:449–454
Shakila RJ, Vasundhara TS, Vijaya Rao D (1996) Inhibitory effect of spices on in vitro histamine production and histidine decarboxylase activity of Morganella morganii and on the biogenic amine formation in mackerel stored at 30°C. Z Lebensm Unters Forsch 203:71–76
Clinical and Laboratory Standards Institute (2015) M07-A10: Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Clinical and Laboratory Standards Institute, Wayne, PA
Klausen NK, Huss HH (1987) A rapid method for detection of histamine-producing bacteria. Int J Food Microb 5:137–146
Özogul F (2011) Effects of specific lactic acid bacteria species on biogenic amine production by foodborne pathogen. Int J Food Sci Tech 46:478–484
Özogul F (2004) Production of biogenic amines by Morganella morganii, Klebsiella pneumoniae and Hafnia alvei using a rapid HPLC method. Eur Food Res Technol 219:465–469
Ceylan E, Fung DYC (2004) Antimicrobial activity of spices. J Rapid Meth Aut Mic 12:1–55
Aliakbarlu J, Mohammadi S, Khalili S (2014) A Study on antioxidant potency and antibacterial activity of water extracts of some spices widely consumed in Iranian diet. J Food Biochem 38:159–166
Fazeli MR, Amin G, Attari MMA, Ashtiani H, Jamalifar H, Samadi N (2007) Antimicrobial activities of Iranian sumac and avishan-e shirazi (Zataria multiflora) against some food-borne bacteria. Food Control 18:646–649
Venkat RS, Srinivas PV, Praveen B, Hara KK, China RB, Suryanarayana MU, Madhusudana RJ (2004) Antibacterial constituents from the berries of Piper nigrum. Phytomedicine 11:697–700
Milenkovic AN, Stanojevic LP (2021) Black pepper: chemical composition and biological activities. Adv Tech 10:40–50
Ahmad I, Mehmood Z, Mohammad F (1998) Screening of some Indian medicinal plants for their antimicrobial properties. J Ethnopharmacol 62:183–193
Wendakoon CN, Sakaguchi M (1992) Effect of spices on growth of and biogenic amine formation by bacteria in fish muscle. Dev Food Sci 30:305–313
Emborg J, Laursen BG, Dalgaard P (2005) Significant histamine formation in tuna (Thunnus albacares) at 2 °C — effect of vacuum- and modified atmosphere-packaging on psychrotolerant bacteria. Int J Food Microb 101:263–279
Lakshmanan PT (2000) Fish spoilage and quality assessment. In: Gopalakrishna Iyer TS et al (eds) Quality assurance in seafood processing. Society of Fisheries Technologists, Cochin, India
Nasar-Abbas SM, Halkman AK, Al-Haq MI (2004) Inhibition of some foodborne bacteria by alcohol extract of sumac (Rhus coriaria L.). J Food Saf 24:257–267
Kosar M, Bozan B, Temell F, Baser KHC (2006) Antioxidant activity and phenolic composition of sumac Rhus coriaria extracts. Food Chem 103:952–959
Gabr SA, El-Metwally MM, Al-Ghadir AH (2014) Antioxidant and antibacterial active constituents of Rhus coriaria. Biotechnology 13:37–45
Singh N, Yadav SS, Kumar S, Narashiman B (2021) A review on traditional uses, phytochemistry, pharmacology, and clinical research of dietary spice Cuminum cyminum L. Phytother Res 35:5007–5030
Merah O, Sayed-Ahmad B, Talou T, Saad Z, Cerny M, Grivot S, Evon P, Hijazi A (2020) Biochemical composition of cumin seeds, and biorefining study. Biomolecules 10:1–18
Alberto MR, Arena ME, Manca de Nadra MC (2007) Putrescine production from agmatine by Lactobacillus hilgardii: effect of phenolic compounds. Food Control 18:898–903
Acknowledgements
The project was funded by the Scientific Research Projects Unit of Cukurova University (Project No: FYL-2015-4813). The authors are grateful for their financial support. This work is also based upon the work from COST Action 18101 SOURDOMICS—Sourdough biotechnology network towards novel, healthier and sustainable food and bioprocesses (https://sourdomics.com/; https://www.cost.eu/actions/CA18101/), where the author J.M.F.R. is the Chair and Grant Holder Scientific Representative and the author F.Ö. is the leader of the working group 8 “Food safety, health promoting, sensorial perception and consumers’ behaviour”, and is supported by COST (European Cooperation in Science and Technology) (https://www.cost.eu/). COST is a funding agency for research and innovation networks. Regarding the author J.M.F.R., this work was also financially supported by: (i) LA/P/0045/2020 (ALiCE) and UIDB/00511/2020–UIDP/00511/2020 (LEPABE) funded by national funds through FCT/MCTES (PIDDAC); (ii) Project PTDC/EQU-EQU/28101/2017–SAFEGOAL—Safer Synthetic Turf Pitches with Infill of Rubber Crumb from Recycled Tires, funded by FEDER funds through COMPETE2020—Programa Operacional Competitividade e Internacionalização (POCI) and by national funds (PIDDAC) through FCT/MCTES.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Compliance with ethics requirements
This manuscript is in compliance with ethical requirements.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Özogul, F., Küley, E., Küley, F. et al. Impact of sumac, cumin, black pepper and red pepper extracts in the development of foodborne pathogens and formation of biogenic amines. Eur Food Res Technol 248, 1803–1813 (2022). https://doi.org/10.1007/s00217-022-04006-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00217-022-04006-x