REVIEW article

Front. Microbiol., 21 September 2016

Sec. Food Microbiology

Volume 7 - 2016 | https://doi.org/10.3389/fmicb.2016.01394

Beneficial Effects of Spices in Food Preservation and Safety

  • 1. Department of Agricultural and Food Sciences, Alma Mater Studiorum, University of Bologna Cesena, Italy

  • 2. Faculty of Biology, Institute of Botany and Botanical Garden “Jevremovac”, University of Belgrade Belgrade, Serbia

  • 3. Division of Cancer Medicine, Department of Experimental Therapeutics, The University of Texas MD Anderson Cancer Center Houston, TX, USA

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Abstract

Spices have been used since ancient times. Although they have been employed mainly as flavoring and coloring agents, their role in food safety and preservation have also been studied in vitro and in vivo. Spices have exhibited numerous health benefits in preventing and treating a wide variety of diseases such as cancer, aging, metabolic, neurological, cardiovascular, and inflammatory diseases. The present review aims to provide a comprehensive summary of the most relevant and recent findings on spices and their active compounds in terms of targets and mode of action; in particular, their potential use in food preservation and enhancement of shelf life as a natural bioingredient.

Introduction

Plant, animal, and microbes represent an unlimited source of compounds with medicinal properties (Tajkarimi et al., 2010). Since ancient time, humans are using spices as nutritional agents (Kaefer and Milner, 2008). According to the U.S. Food and Drug Administration (FDA), spice is an “aromatic vegetable substance in the whole, broken, or ground form, the significant function of which in food is seasoning rather than nutrition” and from which “no portion of any volatile oil or other flavoring principle has been removed” (Sung et al., 2012).

More than 100 varieties of spices are produced throughout the world. Asia is the main leader for the production of spices, particularly of cinnamon, pepper, nutmeg, cloves, and ginger, while Europe grows mainly basil, bay leaves, celery leaves, chives, coriander, dill tips, thyme, and watercress. In America, instead, pepper, nutmeg, ginger, allspice, and sesame seed are mainly produced (Prasad et al., 2011).

Although spices have been used (mostly dried seed, fruit, root, bark, or vegetative material) for rituals, cosmetics and perfumery, their flavoring, coloring and, especially, preservative properties have founded wide applications both in the traditional food preparations and in the food industry. In fact, many compounds isolated from spices (Table 1) have shown antimicrobial activity against some of the most common microorganisms that affect the food quality and shelf life (Tajkarimi et al., 2010). The introduction of spices through the meals has various beneficial effects as well. For instance, they can stimulate the secretion of saliva, promote the digestion, prevent from cold and influenza, and reduce nausea and vomiting (Ravindran, 2002; Sultana et al., 2010). In this manuscript we provide an overview on spices and their constituent as a natural food preservatives in vitro and in vivo.

Table 1

Scientific/Common nameMajor compoundsMicroorganisms/ModelReferences
1. Acacia victoriae (Wattleseed)Avicin, SaponinsS. cerevisiaeSimons et al., 2006
2. Aframomum meleguetaGingerolA. niger, Salmonella spp.,Nneka and Jude, 2012
(Grains of paradise)E. coliJuliani et al., 2008
3. Aframomum corrorima (Korarima)1,8-Cineole, Sabinene,A. flavus, Penicillium expansumHymete et al., 2006
NerolidolE. coli, Salmonella spp.Eyob et al., 2008
Klebsiella spp.Doherty et al., 2010
4. Allium sativum (Garlic)Diallyl sulfide, AllicinSt. aureus, S. Typhi,Yadav and Singh, 2004
B. cereus, B subtilis
E. coli, Ls. monocytogenes,
5. Allium schoenoprasum (Chives)Allicin, Diallyl sulfidesE. coliRattanachaikunsopon and Phumkhachorn, 2008
Shirshova et al., 2013
6. Alkanna tinctoria (Alkanet)Pulegone, 1,8-Cineole,—–Ozer et al., 2010
α-Terpinyl acetate, Isophytol,—–Prasad et al., 2011
Alkannin, Shikonin
7. Alpinia galanga (Greater galanga)Galango-isoflavonoid,S. Typhimurium, St. aureusKaushik et al., 2011
β-Sitosterol, Galangin,B. subtilis, A. niger
β-Caryophyllene, β-SelineneLs. monocytogenes
8. Amomum subulatum (Black cardamom)——-E. coli, P. aeruginosaBhatt et al., 2014
9. Angelica archangelica (Angelica)α-Pinene, δ-3-Carene,E. coli, St. aureusFraternale et al., 2014
Limonene, PhellandreneRather et al., 2013
10. Anethum graveolens (Dill)Carvone, Limonene,Clostridium botulinum,Peerakam et al., 2014
Myristicin, Anethole, EugenolP. aeruginosa,Ceylan and Fung, 2004
St. aureus, Y. Enterocolitica
11. Apium graveolens (Celery seed)β-Pinene, CampheneSt. aureus, E. coliBaananou et al., 2013
Cumene, LimoneneP. aeruginosa
12. Armoracia rusticana (Scherb)Isothiocyanate, CatechinB. subtilis, St. aureusMucete et al., 2006
Kaempferol, Quercetin,Prasad et al., 2011
13. Artemisia dracunculus (Tarragon)Artemisinin Phenolic acidsSt. aureusObolskiy et al., 2011
Coumarins, Flavonoids,Ls. monocytogenes
P. aeruginosa
14. Boesenbergia rotunda (Fingerroot)Pinostrobin, Pinocembrin,Ls. monocytogenesEng-Chong et al., 2012
Cardamonin, Boesenbergin AB. cereus, St. aureus
Boesenbergin BLactobacillus plantarum
Camphor, Linalool, CampheneL. cellobiosus, C. albicans
15. Brassica juncea (Brown mustard)Isothiocyanate, Diallyl trisulfide,Ls. monocytogenes, St. aureus
Allyl- isothiocyanateS. enteritidis, S. veneziana,Miceli et al., 2014
En. hormaechei, En. cloacae,Anuradha et al., 2012
Citrobacter freundii, K. pneumoniaeSethi et al., 2013
En. sakazakii, En. amnigenus
16. Brassica nigra (Black mustard)Gallic acid, Rutin, Caffeic acidE. coli, St. aureusBhatia and Sharma, 2012
Quercetin, Ferulic acidRajamurugan et al., 2012
17. Bunium persicum (Black cumin)γ-Terpinene, CuminaldehydeB. subtilis, St. aureusMazidi et al., 2012
ρ-Cymene, LimoneneGhderi et al., 2014
18. Capsicum annuum (Chilli pepper)CapsaicinSt. aureus, S. TyphimuriumKoffi-Nevry et al., 2012
19. Carum carvi (Caraway)Carvone, Limonene,E. coli, P. aeruginosaAgrahari and Singh, 2014
Carvacrol, Anethole
20. Cinnamomum aromaticum (Cassia)Cinnamaldehyde, EugenolE. coli, S. TyphimuriumBansode, 2012
Ls. monocytogenes
P. aeruginosa, S. enteritidisFrankova et al., 2014
21. Cinnamomum burmanniiGalacturonic acidSt. aureus, E. coliAl-Dhubiab, 2012
(Indonesian cinnamon)Cinnamyl alcohol, CoumarinB. cereus, S. anatum
CinnamaldehydeLs. monocytogenes
22. Cinnamomum verum (Cinnamon)Cinnamic aldehyde, EugenolYadav and Singh, 2004
E. coli, Ps. fluorescensUnlu et al., 2010
Naveed et al., 2013
23. Citrus hystrix (Kaffir lime)Limonene, Citronellal,E. coli, B. cereusTabassum and Vidzasagar, 2013
β-PineneSt. aureus
Ng et al., 2011
24. Ceratonia siliqua (Carob tree)Nonadecane, HeneicosaneLs. monocytogenesHsouna et al., 2011
Farnesol, CamphorB. cereus, St. aureus
E. coli, P. aeruginosa
25. Citrus aurantifolia (Lime)Limonene, β-PineneSt. aureus, A. nigerPathan et al., 2012
γ-Terpinene, CitralSpadaro et al., 2012
26. Coriandrum sativum (Coriander)Dodecenal, 1-DecanolS. epidermidis, St. aureusBharti et al., 2012
ErgosterolP. aeruginosa,Zhu et al., 2011
27. Crocus sativus (Saffron)Lauric acid, Hexadecanoic acid,E. coli, B. subtilisSethi et al., 2013
4-Hydroxy dihydro-Ps. fluorescens, St. aureusZheng et al., 2011
-2(3H)-furanone,C. freundiiBhargava, 2011
Stigmasterol, Crocetin, Crocin
28. Curcuma longa (Turmeric)CurcuminS. Typhi, Ls. monocytogenesMoghadamtousi et al., 2014
Clostridium spp.Radwan et al., 2014
St. aureus, E. coli, B. cereus,
B. subtilis, C. albicans,
Y. enterocolitica, P. notatum,
S. cerevisiae
29. Cuminum cyminum (Cumin)CuminalB. cereus, B. subtilis,Ceylan and Fung, 2004
Ls. monocytogenes,Jirovetz et al., 2005
C. freundii, K. pneumoniaeSethi et al., 2013
Ps. fluorescens,
S. enteritidis, St. aureus
A. niger, S. cerevisiae
C. albicans
30. Cymbopogon citrates (Lemon grass)Citral, Myrcene, Linalool,E. coli, C. albicans,Prasad et al., 2011
FarnesolTyagi and Malik, 2010b
Vazirian et al., 2012
31. Elettaria cardamomum1,8-Cineole, LinaloolB. cereus, Ls. monocytogenesSavan and Kucukbay, 2013
(Green cardamom)α-Terpinyl acetateSt. aureus, S. enteritidisMalti et al., 2007
P. aeruginosa
32. Eruca sativa (Rocket)Erucic acid, Oleic acidS. aureus, S. epidermidisGulfraz et al., 2011
P. aeruginosa
33. Eryngium foetidumE-2-Dodecenal (“eryngial”)St. aureus, B. subtilisShavandi et al., 2012
(Long coriander)Dodecanoic acidLs. monocytogenesNgang et al., 2014
Sharon et al., 2007
34. Ferula asafetidaα-Pinene, α-Terpineol, AzuleneE. coli, B. subtilisMahendra and Bisht, 2012
(Asafoetida)P. chrysogenum, A. ochraceusDivya et al., 2014
35. Foeniculum vulgare (Fennel)AnetholeB. cereus, S. enteritidis,Ceylan and Fung, 2004
Y. enterocoliticaShahat et al., 2011
St. aureus, B. subtilis
E. coli, P. aeruginosa
A. niger, C. vulgaris
Shigella dysenteriae, E. coli
36. Garcinia indica (Kokum)GarcinolE. coli, B. cereusElumalai and Eswaraiah, 2011
St. aureus, C. albicans
37. Heracleum persicum (Golpar)Pimpinellin, IsopimpinellinC. albicansHemati et al., 2010
Bergapten, IsobergaptenSt. aureus
38. Hyssopus officinalis (Hyssop)Isopinocamphone, Terpinen-4-olE. coli, S. Typhimurium,Di Pasqua et al., 2005
Pinocarvone, CarvacrolC. albicans, S. aureusSüleyman et al., 2010
39. Houttuynia cordataAristolactams, Houttuynoside AS. TyphimuriumKumar et al., 2014
(Chameleon plant)Quercitrin, Quercetin-3-O-β-D-
-galactopyranoside
40. Illicium verum (Star anise)Shikimic acid, AnetholeB. cereusShan et al., 2007
41. Kaempferia galanga (Kencur)Ethyl-cinnamate, 1,8-cineoleSt. aureus, E. coliUmar et al., 2011
Camphene, Borneol, KaempferolC. albicans
Kaempferide
42. Laurus nobilis (Bay)1,8-Cineole, α-Pinene, LimoneneAlternaria alternata, E. coliXu et al., 2014
2-CareneCherrat et al., 2014
43. Lavandula angustifolia1,8-Cineole, Camphor, BorneoleSt. aureusCavanagh and Wilkinson, 2005
(Lavender)P. aeruginosa, E. coliTorabbeigi and Azar, 2013
44. Limnophila aromaticOcimene, Terpinolene, CamphorSt. aureus, B. cereusGorai et al., 2014
(Finger grass)S. epidermidis
45. Lippia adoensis (Koseret)Linalool, Germacrene DSt. aureus, C. albicansFolashade and Egharevba, 2012
S. cerevisiae
46. Lippia graveolensThymol, Carvacrol, flavonoidsM. luteus, Salmonella spp.Hernández-Hernández et al., 2014
(Mexican oregano)Aspergillus niger
Herpes simplex virus
human respiratory syncytial virus
and human rotavirusPilau et al., 2011
47. Maranta arundinacea (Arrowroot)Flavonoids, terpenoidsE. coli, Ls. monocytogenes,Kim and Fung, 2003
S. enteritidis, St. aureusRajashekhara et al., 2013
48. Melissa officinalis (Balm)Neral, Citronellal, Isomenthone,
Menthone, β-Caryophyllene,Shigella sonneiMoradkhani et al., 2010
Carvacrol
49. Mentha piperita (Mint)Menthol; 1,8-cineoleE. coli, P. aeruginosa, St. aureus,Sharafi et al., 2010
Streptococcus faecalis, C. albicansSaharkhiz et al., 2012
McKay and Blumberg, 2006
Tyagi et al., 2013
50. Monodora myristicaCymene, α-PhellandreneSt. aureus, B. cereusOwokotomo and Ekundayo, 2012
(Calabash nutmeg)Germacrene D-4-olC. albicans
Odoh et al., 2004
51. Murraya koenigiiMurrayanol
(Curry leaf)Murrayacine, MahanineStaphylococus sp.Handral et al., 2012
52. Myrica gale (Gale)Cymene, β-Elemene,St. aureus, B. subtilisNakata et al., 2013
Myrcene, LimoneneS. cerevisiae, C. albicans
53. Myristica fragransMyristicin, SabineneSt. aureus, B. subtilisGupta et al., 2013b
(Nutmeg)β-PineneP. aeruginosa, A. nigerRadwan et al., 2014
Clostridium spp.
54. Myrrhis odorata (Cicely)p-Cymene, α-Terpinene,E. coli, St. aureus,Rancic et al., 2005
δ-CadineneC. albicans, A. niger
55. Myrtus communis (Myrtle)Myrtenyl acetate, 1,8-Cineole,Ls. monocytogenesAmensour et al., 2010
α-PineneP. aeruginosaCherrat et al., 2014
56. Nigella sativa (Black caraway)Thymoquinone, NigelloneSt. aureusIslam et al., 2012
E. coli, P. aeruginosa
57. Ocimum canumα-Terpineol, Chavicol,Food spoiling bacteriaVyry Wouatsa et al., 2014
Chavibetol
58. Ocimum basilicum (Basil)1,8-CineoleB. subtilis, E. coli,Moghaddam et al., 2011
Linalool, Methyl chavicolS. Typhimurium, S. aureusShirazi et al., 2014
Ls. monocytogenes,Burt, 2004;
Cl. botulinumShirazi et al., 2014
Ls. innocua, Ps. fragi,Alves-Silva et al., 2013
Ps. fluorescens, Yarrowia lipolytica
C. albicans
59. Olea europaea (Olive)OleuropeinB. cereus, E. coliFaiza et al., 2011
El and Karakaya, 2009
60. Olax subscorpioidea———–C. albicans, C. tropicalisDzoyem et al., 2014
61. Origanum vulgare (Oregano)CarvacrolE. coli,
Ls. monocytogenesSiroli et al., 2014b
S. cerevisiaeLv et al., 2011
Ls. monocytogenes
62. Origanum majorana———–B. subtilis, E. coliLeeja and Thopil, 2007
(Marjoram)P. aeruginosa, St. aureus
A. niger
63. Pandanus amaryllifolius2-Acetyl-1-pyrrolineE. coliRoutray and Rayaguru, 2010
(Pandan leaves)Faras et al., 2014
64. Petroselinum crispumKaempferol, QuercetinB. cereus, St. aureus,Haidaria et al., 2011
(Parsley)Ls. monocytogenesShan et al., 2007
65. Persicaria odorataβ-Caryophyllene,St. aureus, E. coliShavandi et al., 2012
(Vietnamese coriander)β-Caryophyllene,Sasongko et al., 2011
Caryophyllene oxide
66. Pimpinella anisum (Anise)AnetholeA. ochraceusKrisch et al., 2011
Fusarium moniliforme
67. Piper betle (Betel)Eugenol, AcetyleugenolSt. aureus, E. coliPrakash et al., 2010
Vibrio choleraeHoque et al., 2011
68. Piper capense (Timiz)β-Pinene, SabineneSt. aureusWoguem et al., 2013
69. Piper guineenseLignans, Amides, Alkaloids,St. aureus, E. coliNwinyi et al., 2009
(Ashanti pepper)Flavonoids, PolyphenolsJuliani et al., 2013
70. Piper nigrum (Black peper)PiperineSt. aureus, E. coliShiva Rani et al., 2013
B. cereus, P. aeruginosa
71. Piper retrofractumPiperineE. coli, P. aeruginosaKhan and Siddiqui, 2007
(Long pepper)A. niger
72. Polygonum hydropiperCatechin, Polygodial,E. coli, B. subtilisMoyeenul Huq et al., 2014
(Water-pepper)Quercetin, HyperinSt. aureus
S. cerevisiae, C. albicans
73. Quassia amara (Amargo)QuassinE. coli, St. aureusAjaiyeoba and Krebs, 2003
Cachet et al., 2009
74. Rhus coriaria (Sumac)Quercetin, Myricetin, KaempferolE. coli, St. aureusShabir, 2012
Gallic acid, Methyl gallateLs. monocytogenes
m-Digallic acid, Ellagic acid
75. Rosmarinus officinalisp-Cymene, Linalool,Jayasena and Jo, 2013
(Rosemary)Thymol, γ-Terpinene,Brochothrix thermosphactaÖzcan and Chalchat, 2008
Carnosic acid, CarnosolPseudomonas spp.De La Torre Torres et al., 2015
76. Ruta graveolens (Rue)RutinSt. aureus, E. coliHamad, 2012
Kumar et al., 2014
77. Salvia officinalis (Sage)1,8-CineoleSalmonella sp.Hayouni et al., 2008
78. Sanguisorba minor (Salad burnet)Linalool, β-sitosterolE. coli, St. aureusEsmaeili et al., 2010
79. Sassafras albidum (Sassafras)Safrole, Camphor,P. aeruginosa,Kamdem and Douglas, 2007
Methyl eugenolS. TyphimuriumBarbosa et al., 2012
80. Satureja hortensis (Summer savory)Carvacrol, γ-terpinene, p-cymeneB. subtilis, P. aeruginosa,Mihajilov-Krstev et al., 2010
C. albicans, S. cerevisiae
81. Satureja montanaCarvacrol, tannins, flavonoids,Carraminana et al., 2008
(Winter savory)triterpenesLs. monocytogenes
82. Schinus terebinthifoliusSchinol, QuercetinSt. aureus, B. cereusCarvalho et al., 2013
(Brazilian pepper)Degaspari et al., 2005
83. Sesamum indicum (Sesame)Latifonin, Momor-cerebroside,E. coliOgunsola and Fasola, 2014
Soya-cerebrosideHu et al., 2007
84. Sinapis alba (White mustard)Benzyl isothiocyanateE. coliAl-Qudah et al., 2011
Benzyl nitrile, thymol
85. Smyrnium olusatrumSabinene, Curzerene———-Mokaddem et al., 2010
(Alexanders)α-Pinene, Cryptone
86. Syzygium aromaticumEugenolE. coli, St. aureusYadav and Singh, 2004
(Clove)S. anatum, B. cereusNaveena et al., 2006
C. freundii, K. pneumoniaeShan et al., 2007
Sethi et al., 2013
87. Tagetes minutacis-β-ocimeneE. coli, B. cereus, B. subtilisSadia et al., 2013
(Huacatay)St. aureus, Ps. aeruginosa, S. TyphySenatore et al., 2004
C. albicansShirazi et al., 2014
88. Tasmannia lanceolataPolygoidal, Safrole,St. aureusCock, 2013
(Tasmanian pepper)Guaiol, Calamenene,E. coli, S. TyphimuriumWeerakkody et al., 2010
Myristicin, DrimenolLs. monocytogenes
A. niger, C. albicans
89. Thymus vulgaris (Thyme)Thymol, CinnamaldehydeBurt, 2004
Jayasena and Jo, 2013
Ls. monocytogenes,
P. putida
90. Thymus capitatusThymol, Camphor,B. cereus, Salmonella sp.Boubaker et al., 2013
(Headed Savory)CarvacrolLs. innocuaBounatirou et al., 2007
91. Thymus serpyllumThymol, CarvacrolLs. monocytogenesSkrinjar and Nemet, 2009
(Breckland thyme)St. aureus, E. coliPaaver et al., 2008
92. Trigonella foenum-graecumTrigonellineE. coli, B. cereusUpadhyay et al., 2008
(Fenugreek)Kaempferol 7-O-glucosideOmezzine et al., 2014
93. Trachyspermum ammiβ-Phellandrene, α-Terpinene,C. albicans, Salmonella spp.,Khan et al., 2010
(Ajwan)LimoneneSt. aureus, E. coliChauhan et al., 2012
S. Typhimurium
94. Vanilla planifoliaVanillin, Vanillic acidE. coli, B. cereusMenon and Nayeem, 2013
(Vanilla)S. cerevisiae,Fitzgerald et al., 2003
Zygosaccharomyces bailii, Z. rouxiiShanmugavalli et al., 2009
95. Verbena officinalisCitral, Isobornyl formateE. coli, S. TyphimuriumDi Pasqua et al., 2005
(Vervain)Ls. monocytogenes, S. aureusDe Martino et al., 2008
Lactococcus garvieae, L. plantarum,
L. delbrueckii,
Brochothrix thermosphacta
96. Xylopia aethiopica4-Terpineol, 1,8-CineoleB. cereus, St. aureusFleischer et al., 2008
(Grains of Selim)MyrtenolP. aeruginosa, C. albicansElhassan et al., 2010
Vyry Wouatsa et al., 2014
97. Zanthoxylum bungeanumTerpinen-4-ol, 1,8-Cineole,St. aureusGong et al., 2009
(Chinese prickly ash)LimoneneB. cereus, B. subtilisZhu et al., 2011
Shan et al., 2007
98. Zanthoxylum piperitumSanshoolSt. aureus, E. coliKim et al., 2007
(Japanese pepper)S. Typhimurium
99. Zingiber officinale (Ginger)Gingerol, Shogoal,E. coli, Salmonella spp.Ghosh et al., 2011
Methyl-isogingerolStaphylococci, Streptococci

Antimicrobial potential of phytochemicals (spices) for food preservation; In vitro study.

Importance of spices

Spices have been important to mankind since the beginning of history. Several mythological evidence including “Epic of Gilgamaesh,” and the “Bagavad Gita,” suggest their use for several purposes. Because of their strong preservative quality, spices were also used for embalming. According to Ayurveda, they help to maintain the balance of the body humors (Gupta et al., 2013a). Besides these, spices have been used to change the physical appearance of food. For instance, pepper and turmeric changed the color, appearance and the taste of food with many health benefits. Ginger, nutmeg and cinnamon improve digestion, considered good for spleen and sore throats (Prasad et al., 2011). Unfortunately, this beneficial effect of spices is not clinically proven. However, traditional practices emphasize the health benefits of spices. Eventually, recent studies highlighted other biological functions of spices, including antimicrobial, antioxidant, and anti-inflammatory (Tajkarimi et al., 2010).

Spices for food preservation and safety

Food spoilage refers to an irreversible modification in which food becomes not edible or its quality is compromised. Such changes can be driven by different factors, either physical (oxygen, temperature, light) and/or biological (enzymatic activity and microbial growth). Despite the current technologies available in the production chain (for instance freezing, pasteurization, drying, preservatives), it seems impossible to eliminate completely the risk of food spoilage (Gutierrez et al., 2009). Lipid oxidation is one of the main issues of food spoilage. Hence, food industries have applied antioxidants such as butylated hydroxytoluene (BHT) and butylated hydroxyanisole (BHA) to prevent spoilage (Stoilova et al., 2007). However, their safety is doubtful and consumers are progressively demanding natural compounds. For this reason spices represent a potent tool for the food industry, thanks to their natural properties (Hyldgaard et al., 2012). Indeed spices possess antioxidant capacity, mainly due to the presence of phenolic compounds (Figures 1A,B). They exhibit antioxidant property by scavenging free radicals, chelating transition metals, quenching of singlet oxygen, and enhancing the activities of antioxidant enzymes (Rubió et al., 2013). Stoilova et al. (2007) reported that the CO2 extract of ginger had in vitro activity comparable with that of BHT in inhibiting the lipid peroxidation both at 37 and 80°C. Moreover, pimento and black pepper extracts reduced the formation of acrylamide up to 75 and 50%, respectively, in a model mixture simulating heated potato matrix (180°C for 20 min). Eugenol, the main component of pimento essential oil, limited the formation of acrylamide by 50% (Ciesarová et al., 2008). Some other studied antioxidants are: quercetine (dill), capsaicin (red chilli), curcumin (turmeric), carvacrol (oregano, thyme, marjoram), thymol (oregano, thyme), piperine (black pepper), gingerol, etc (ginger, marjoram; Figures 1A,B; Rubió et al., 2013; Przygodzka et al., 2014; Srinivasan, 2014). The relationship between antioxidant properties of spices and food spoilage has been well-documented.

Figure 1

Figure 1

Chemical structure of bioactive compounds of commonly used spices. (A) Volatile compounds; (B) Not volatile compounds.

Another issue in food spoilage is the microbial growth. Spices can also exert antimicrobial activity in two ways: by preventing the growth of spoilage microorganisms (food preservation), and by inhibiting/regulating the growth of those pathogenic (food safety; Tajkarimi et al., 2010). Studies regarding in vitro and in vivo antimicrobial activities of spices have been reported in the following sections.

Antimicrobial activity In vitro

Numerous articles published in the last few decades have described the antimicrobial activities of spices in vitro. Extracts of entire plants, or part of them, obtained with diverse solvents (such as ethanol, methanol, ethyl acetate, and water) have been tested against microbes (Tajkarimi et al., 2010). Their essential oils or active compounds, alone or in combination, were also used to test the activity against different microbes (Singh et al., 2007; Weerakkody et al., 2010; Bassolé and Juliani, 2012). Disc-diffusion, drop-agar-diffusion, broth microdilution, and direct-contact technique in agar represent the most common methods utilized for screening (Tyagi and Malik, 2010a, 2011).

According to these reports, spices possess a very wide spectrum of activity against Gram-positive and Gram-negative bacteria, yeasts and molds (Tajkarimi et al., 2010; Table 1). Alves-Silva et al. (2013) reported that the bush-basil essential oils have antimicrobial activity against Listeria innocua, Serratia marcenscens, Pseudomonas fragi, P. fluorescens, Aeromonas hydrophila, Shewanella putrefaciens, Achromobacter denitrificans, Enterobacter amnigenus, En. gergoviae, and Alcaligenes faecalis, and against the yeasts Yarrowia lipolytica, Saccharomyces cerevisiae, Candida zeylanoides, Debaryomyces hansenii, and Pichia carsonii. Moreover, they were able to inhibit molds such as Mucor racemosus and Penicillium chrysogenum. In the same study, celery and coriander essential oils also showed a very similar antimicrobial activity against the tested strains.

Although the antimicrobial activity of spices may vary according to the types of spice (origin and bioactive compounds), different bacteria can react in different ways (Hyldgaard et al., 2012). Oregano essential oil showed higher antimicrobial activity against Listeria monocytogenes compared to Escherichia coli (Siroli et al., 2014b). Huacatay and basil essential oils were active against Staphylococcus aureus and Bacillus subtilis (Shirazi et al., 2014). Essential oil of angelica roots were effective against Clostridium difficile, Cl. perfringens, Enterococcus faecalis, Eubacterium limosum, Peptostreptococcus anaerobius, and in a lower extent against E. coli and Bacteroides fragilis (Fraternale et al., 2014). Nigella sativa extracts were more effective on St. aureus (5th day inhibition zone 34 mm) as compared to E. coli (5th day inhibition zone, 13 mm) and P. aeruginosa (5th day inhibition zone, 30 mm; Islam et al., 2012). Rosmarinus officinalis essential oil showed a strong antimicrobial effect against Ls. monocytogenes and S. aureus compared with E. coli (Jordán et al., 2013). A list of spices and their effects on most relevant bacteria is reported in Table 1.

Spices, essential oils and extracts have also been known for their anti-fungal activity (Table 1; Tajkarimi et al., 2010). Huacatay and basil essential oils were active against Candida albicans (Shirazi et al., 2014). Radwan et al. (2014) reported that among 22 common spice extracts, turmeric, and nutmeg extracts were the most active against different plant pathogens belonging to the genus Colletotrichum. In another study, where 23 spice extracts were studied, Olax subscorpioidea extract showed the highest antifungal activity, particularly against C. albicans and C. tropicalis (Dzoyem et al., 2014). A reduction of mycelial growth and inhibition of conidial germination and aflatoxin production by A. flavus were described by Nerilo et al. (2016) when 150, 10 and 15 μg/mL of ginger EO were applied, respectively. Ferreira et al. (2013) also reported a decrease (99.9 and 99.6%) of aflatoxin B1 and B2 when 0.5% of turmeric EO was employed while the same EO completely inhibited the biomass of Fusarium graminearum and its zearalenone production, at 3.5 and 3 mg/mL, respectively (Kumar et al., 2016).

Finally, antiviral activity of Mexican oregano against some viruses (i.e., acyclovir-resistant herpes simplex virus type 1 (ACVR-HHV-1), human respiratory syncytial virus (HRSV), and human rotavirus) has been reported (Pilau et al., 2011). Overall, it is difficult to predict how microorganisms are susceptible. In fact, spics constituents may impact several targets, such as microorganisms cell membrane, enzymes, and/or their genetic material (through the modulation of specific genes; Tajkarimi et al., 2010; Tyagi and Malik, 2010b,c; Hyldgaard et al., 2012).

Enhancement of the antimicrobial activity in vitro

To enhance the antimicrobial potential of spices or their constituents, the use of mixed extracts or natural compounds having different origins have been reported (Bassolé and Juliani, 2012). In most of the cases spices showed synergistic activities/effects. For instance, the antimicrobial activity of basil, oregano, bergamot, and perilla essential oils alone or in combinations, were tested. Basil and oregano essential oils alone had MICs of 1.25 and 0.625 μL/mL against E. coli, respectively, while their values were 0.313 μL/mL when used in combination. The MIC values against St. aureus for basil and bergamot EOs alone were for both 1.25 μL/mL, whereas the MICs of the two essential oils decreased to 0.313–0.156 μL/mL when combined, indicating higher antimicrobial activity. MICs of oregano and bergamot essential oils were 0.625 and 1.25 μL/mL against B. subtilis, respectively, whereas 0.313 μL/mL was determined for combined effect. Finally, the MIC values of oregano and perilla were 0.625 μL/mL for both against S. cerevisiae, while the mixture needed MICs of 0.313–0.156 μL/mL (Lv et al., 2011). In another study, Tabanelli et al. (2014) demonstrated the additive effect of citral and linalool against S. cerevisiae. In fact, linalool (250 mg/L) reduced markedly the amount of citral needed for the same effect (from around 150 to 50 mg/L). However, Tejeswini et al. (2014) reported antagonistic effects when cinnamaldehyde was combined with clove essential oils for molds inhibition.

The use of spice oils together with other preservation techniques has been also assessed. For example, low pressure atmosphere enhanced the susceptibility of E. coli and S. enteritidis to oregano, lemongrass or cinnamon essential oils in vitro. In particular, the MIC of cinnamon vapors for S. enteritidis decreased from 0.512 to 0.128 μL/mL (Frankova et al., 2014). Tabanelli et al. (2014) reported that the decrease of aw potentiated the antimicrobial effect of citral (but not linalool) while lower pH favored the antimicrobial power of linalool (but not citral) against S. cerevisae. Some other hurdle technologies were also used for the enhancement of antimicrobial potential of essential oils. Tyagi and Malik (2010a, 2011, 2012) described the enhancement in antimicrobial potential of essential oils in combination of negative air ions (NAI) against food spoilage microorganisms.

Antimicrobial potential in real food model system (In vivo)

Numerous natural compounds of spices with defined antimicrobial properties have been isolated. However, in vitro studies represent only one part of the use of active compounds as preservatives in food. Moreover, their physical and biochemical properties have been changed in real food systems due to the complexity of the food matrices (Tajkarimi et al., 2010). Therefore, whether spices or their components have the potential to inhibit the food spoilage and act as a food preservative has been determined in different studies.

As summarized in Table 2, the use of spices as preservatives has been assessed in multiple foods: meat, fish, dairy products, vegetables, rice, fruit, and animal food (Tajkarimi et al., 2010; Jayasena and Jo, 2013). Hernández-Ochoa et al. (2014) reported that cumin and clove essential oils inhibited the growth of total bacteria by 3.78 log CFU/g when used on meat samples for 15 days at 2°C. The antimicrobial activity of different spice extracts in raw chicken meat during storage for 15 days at 4°C was also studied. It has been found that the treatment of raw chicken meat with extracts of clove, oregano, cinnamon, and black mustard was effective against microbial growth (Radha et al., 2014). Essential oils of marjoram and coriander showed above 50% protection of chickpea seed from Aspergillus flavus infestation (Prakash et al., 2012). In an in vivo assay with cherry tomatoes (Lycopersicon esculentum), bay oil was effective against Alternaria alternata infection (Xu et al., 2014). In another experiment, Da Silveira et al. (2014) treated fresh Tuscan sausages with bay leaf essential oil. Comparing to the non-treated control, the essential oil was able to reduce the population of total coliforms (reduction of 2.8 log CFU/g) and extended the shelf life for 2 days. Rattanachaikunsopon and Phumkhachorn (2008) applied basil oil in nham, a fermented pork sausage, inoculated with S. enteritidis SE3 at 4°C. Basil oil reduced the number of bacteria from 5 to 2 log CFU/g after 3 days and the sensory evaluation suggested that these concentrations of oil were acceptable for the consumers. The isothiocyanates derived from oriental mustard reduced aflatoxins biosynthesis in A. parasiticus by 60.5–89.3% during Italian piadina storage (Saladino et al., 2016). Finally, Patrignani et al. (2015) reviewed the use of spices and their constituents in minimally processed fruits and vegetables.

Table 2

Scientific/Common nameReal food modelsReferences
1. Allium sativumPrevent infections of L. acidophlus, E. coliYadav and Singh, 2004
and Aer omonas hydrophila in poultry meat
2. Artemisia dracunculusInhibit growth St. aureus and E. coli in cheeseRaeisi et al., 2012
3. Boesenbergia rotundaRetard the growth of total viable counts of food pathogen
bacteria bacteria in Chinese sausageKingchaiyaphum and Rachtanapun, 2012
4. Brassica nigraReduce microbial growth in raw chicken meatRadha et al., 2014
5. Cinnamomum verumPotential bio preservative of banana, vegetables, dairy productsSessou et al., 2012
against Aspergillus spp., Salmonella spp.,
6. Citrus hystrixInhibit the growth food pathogen bacteria in Chinese sausageKingchaiyaphum and Rachtanapun, 2012
7. Ceratonia siliquaInhibit the growth of Ls. monocytogenes in minced beef meatHsouna et al., 2011;
8. Coriandrum sativumProtection of chickpea seed from A. flavus infestationPrakash et al., 2012
9. Cuminum cyminumCumin seed oil protect stored protection of wheatKedia et al., 2014
and chickpea against Aspergillus spp.
reduce total bacteria in meat samplesHernández-Ochoa et al., 2014
10. Cymbopogon citratusInhibit the growth B. cereus, S. Typhimurium and St. au reus/
antibacterial agents in refrigerated chicken pattiesHayam et al., 2013
control Ls. monocytogenes in bovine ground meatDe Oliveira et al., 2013
inhibit microbial growth in real food systemTyagi et al., 2013
Tyagi et al., 2014a
11. Cinnamomum cassiaRaw chicken meatRadha et al., 2014
in Fresh sliced apples reduces natural microfloraPatrignani et al., 2015
and inoculated Ls. innocua
12. Eryngium foetidumReduce the growth of Ls. monocytogenes in pineapple juiceNgang et al., 2014
13. Laurus nobilisBay essential oil reduce the population of total coliforms in fresh sausagesDa Silveira et al., 2014
Protects cherry tomatoes against Alternaria alternata infectionXu et al., 2014
14. Mentha piperitaMentha essential oil inhibit S. cerevisiae growth inTyagi et al., 2013
fruit (orange/apple) juice-potential natural food preservative
15. Olea europaeaAntibacterial effect against E. coli, P. aeruginosa, S. aureus and
K. pneumoniae in shrimp/seafood industryAli et al., 2014
16. Origanum vulgareInhibit the growth of L. monocytogenes, Aeromonas hydrophila
and E. coli O157:H7 in meat, eggplant saladTajkarimi et al., 2010
inhibition of Pseudomonas spp. in rabbit meatTajkarimi et al., 2010
effectively inhibited the growth of Salmonella spp. in chicken meatBurt, 2004
Jayasena and Jo, 2013
effective against microbial growth in raw chicken meatRadha et al., 2014
in Fresh sliced apples reduces natural microflora and inoculated Ls. InnocuaPatrignani et al., 2015
Inhibit E coli O157:H7 in egg plant saladPatrignani et al., 2015
inhibit Ls. monocytogenes, Y. enterocolitica, and A. hydrophilla in Iceberg lettucePatrignani et al., 2015
control the natural microflora and inhibit Ls. monocytogenes,Patrignani et al., 2015
E. coli in Lamb's lettuce
17. Origanum majoranaProtection of chickpea seed from A. flavus infestationPrakash et al., 2012
18. Ocimum basilicumInhibit the growth of S. enteritidis in fermented pork sausageRattanachaikunsopon and Phumkhachorn, 2008
19. Piper nigrumOil and oleoresins control microbial growth in orange juiceKapoor et al., 2014
20. Rosmarinus officinalisInhibit the growth of Ls. monocytogenes, Aeromonas hydrophila
and E. coli O157:H7 in meatTajkarimi et al., 2010
inhibition effect on Ls. monocytogenes in liver pork sausageTajkarimi et al., 2010
inhibit Ls. monocytogenes, Y. enterocolitica and A. HydrophillaPatrignani et al., 2015
in iceberg lettuce
21. Salvia officinalisInhibit food spoilage in dairy productsTajkarimi et al., 2010
and Salmonella spp. in minced beef meatHayouni et al., 2008
22. Satureja montanaControl the growth of foodborne bacteria/improve quality of minced porkTajkarimi et al., 2010
23. Syzygium aromaticumInhibit the growth of Ls. monocytogenes in mozzarella cheese, meatTajkarimi et al., 2010
and bovine ground meatDe Oliveira et al., 2013
reduced total bacteria in meat samplesHernández-Ochoa et al., 2014
effective against microbial growth in raw chicken meatRadha et al., 2014
24. Thymus vulgarisSlight effect on Ps. putida in cooked shrimp sausagesBurt, 2004
inhibit E. coli O157:H7 growth inhibition in lettuce and carrotsPatrignani et al., 2015
and L. monocytogenes growth inhibition in minced porkBurt, 2004
control the natural microflora and inhibit Ls. monocytogenes,Patrignani et al., 2015
E. coli in lamb's lettuce
25. Thymus capitatusLs. monocytogenes growth inhibition in minced beef meatEl Abed et al., 2014
26. Zingiber officinalePotential biopreservative of beverages against food spoiling yeasts and bacteriaSessou et al., 2012

Antimicrobial potential of phytochemicals (spices) for food preservation; In vivo study.

Although several studies proved possible applications for spices and their derivatives as food preservatives, only few of them are currently applied on the market. For instance, rosemary is already employed for its preservative properties in meat products. Essential oil of rosemary has been used not only for its flavoring compounds but also for its antimicrobial and antioxidant activity. In fact, carnosic acid, one of its main component, is not only antimicrobial but it possesses an antioxidant activity higher than the common food additives, butylated hydroxytoluene (BHT), and butylated hydroxyanisole (BHA; De La Torre Torres et al., 2015).

Allyl isothiocyanate (AITC), a bioactive organosulfur compound found in cruciferous, plants, such as mustard, is known for its anticarcenogenic properties. It has been tested for effectiveness in preservation of fresh beef, sliced raw tuna and cheese. It possesses a strong antimicrobial activity against E. coli O157:H7, Salmonella enterica serovar Montevideo, S. enterica ser. Typhimurium, P. corrugata, Campylobacter jejuni, St. aureus, and Ls. monocytogenes. Moreover it has the generally recognized as safe (GRAS) status provided by the regulatory agencies of U.S. However, its application is sometimes limited because of its poor aqueous solubility, instability at high temperature, and susceptibility to degradation by nucleophilic molecules (Kim et al., 2002; Li et al., 2015).

Enhancement of the antimicrobial activity In vivo

Although some in vivo studies ended up with products acceptable for the consumers, the sensory aspect represents a critical point in the use of spices and their active compounds in food. In fact, sometimes MIC values were three or four times higher than those estimated in vitro, have been applied to have a measurable or stable antimicrobial effect in vivo. This aspect can dramatically affect the physical characteristics and organoleptic properties of the food products. To overcome these issues, several strategies have been exploited for the enhancement of antimicrobial potential of spices in vivo.

The synergistic effect of spices together with their constituents or other natural products has been tested. Water extracts of clove, cinnamon, and oregano were applied, alone (10 mg/L) or in combination (3.3 g/L each), in raw chicken meat and several characteristics were followed during storage for 15 days at 4°C. The mixture of the three extracts had the strongest impact on the bacterial load due to the synergistic actions of antimicrobial compounds present in the mixed spices (Radha et al., 2014). Siroli et al. (2014a) examined citral, carvacrol, citron essential oil, hexanal and 2-(E)-hexenal, alone (250 mg/L) or in combination (125+125 mg/L, except for the combination of citron essential oil/carvacrol, 200+50 mg/L, respectively), to sanitize minimally processed apples. The treatment with citral/2-(E)-hexenal and hexanal/2-(E)-hexenal maintained a good retention of color parameter within the 35 days and there were no yeast spoilage in any treated sample. Gabriel and Pineda (2014) studied the effect of different concentrations of vanillin and licorice root extract (LRE) on the mild heat decimal reduction times (D55-values) of a cocktail of E. coli O157:H7 in young coconut liquid endosperm. They found that the combined effect was most significant only at concentrations above 250 and 210 mg/L, respectively for vanillin and LRE. The efficacy of thymol (0.1% w/w) in combination with sodium lactate (1 and 2% v/w) was evaluated in fish patty samples stored at 4°C for 5 days. The presence of thymol plus 2% of sodium lactate had a synergetic effect against S. enterica ser. Typhimurium (Ilhak and Guran, 2014). Tejeswini et al. (2014) evaluated the antifungal activity of cinnamaldehyde, eugenol, peppermint, and clove essential oils and their combinations in tomato fruit system. While different concentrations of eugenol in combination with peppermint showed either additive or non-significant effect on mold inhibition, combination of cinnamaldehyde with clove essential oil produced non-significant or antagonist effects. Barbosa et al. (2014) also assessed the impact of basil essential oil alone or in combination with sodium hexametaphosphate (SHMP), on the shelf life of chicken sausage. Concentrations of 0.3 or 0.03% of essential oil inhibited the coliforms for 15 days at 4°C (P < 0.05). On the contrary, this effect was inhibited when SHMP was combined.

The synergistic effect of spices on other food preservation systems, such as mild thermal processing, has been also explored. Ngang et al. (2014) studied how to reduce the thermal impact during juice production. They demonstrated that pasteurizing pineapple juice at 60°C in presence of long coriander essential oil, lowered the time required for a 97% reduction of Ls. monocytogenes compared with treatment without essential oil. Similarly, mint, lemon grass, or eucalyptus essential oils worked synergistically with mild thermal treatment to inhibit the microbial growth in real food systems. Therefore, subsequent lower doses of oils were required for the food preservation (Tyagi et al., 2013, 2014a,b).

The use of spices together with additional high tech/cutting-edge technologies has also been studied. Pina-Pérez et al. (2012) demonstrated the applicability of Pulsed Electric Fields (PEF) in combination with cinnamon against S. enterica ser. Typhimurium to enhance the safety of dairy beverages. The maximum synergistic effect was achieved by 10 kV/cm–3000 μs PEF treatment with 5% (w/v) cinnamon. The maximum inactivation level (1.97 log10 cycles) was achieved at 30 kV/cm–700 μs plus 5% cinnamon. Patrignani et al. (2013) enhanced the effect of high-pressure homogenization (HPH) treatment (100 MPa for 1–8 successive passes) with citral into inoculated apricot juices, extending their shelf life in turn. Abriouel et al. (2014), instead, potentiated the effect of high hydrostatic pressure (HHP) on brined olives using thyme and rosemary essential oils. In other cases, novel technologies have been used to preserve the functional compounds. For instance, the use of AITC can be limited by its poor aqueous solubility, degradation by nucleophilic molecules, high volatility, and strong odor. Koa et al. (2012) masked the odor and volatility of AITC through its microencapsulation with Arabic gum and chitosan. In addition, Li et al. (2015) developed nanoemulsions that allowed a better aqueous solubility and chemical stability. Eventually, new packaging systems (active packaging) have been studied where essential oils or their main compounds were incorporated into the films. However, until now the research did not provide consistent results (Maisanaba et al., 2016). All these studies showed that the antimicrobial and food preservative potential of natural compounds can be enhanced or maintained by applying physical technologies.

Mode of antimicrobial action of spices

Although the antimicrobial effects of spices and their derivates have been tested against a wide range of microorganisms over the years, their mode of action is still not completely understood. In fact, spices and their essential oils can contain many different bioactive compounds present in variable amounts. Basically, the bioactive constituents of spices can be divided into volatile and non-volatile compounds (Figures 1A,B). The first ones are mainly responsible for the antimicrobial activity of spices. They can be divided in four groups: terpens, terpenoids, phenylpropenes, and “others” (such as products of degradation; Hyldgaard et al., 2012). Terpens are evaluated as lesser active antimicrobial compounds amongst the other compounds. For instance, the weak activity of ρ-cymene, one of the main component of thyme, is mainly related to its action as a substitutional membrane impurity. It can affect the melting temperature and the membrane potential, which in turn causes a decrease in cell motility (Hyldgaard et al., 2012). On the other hand, terpenoids, such as the well-studied thymol and carvacrol, exert their antimicrobial activity due to their functional groups (hydroxyl groups and delocalized electrons). For instance, thymol can interact with the membrane both with the polar head-group region of the lipid layer, affecting the permeability, or with the proteins, determining an accumulation of misfolded structures (Hyldgaard et al., 2012; Marchese et al., 2016). These changes can lead to cell leakages that in turn can bring the cell to death (O'Bryan et al., 2015). Once it is inside the cells, thymol can also disrupt important energy-generating processes such as the citrate metabolic pathway and the synthesis of ATP (Hyldgaard et al., 2012; O'Bryan et al., 2015). Carvacrol acts mainly at the level of the membrane as a transmembrane carrier of monovalent cations, exchanging K+ with H+ in the cytoplasm (O'Bryan et al., 2015). Other organic compounds present in spices are phenylpropenes, such as eugenol and cinnamaldhehyde. The antimicrobial activity of eugenol is performed mainly at the level of the membranes and proteins, inducing permeabilization and enzyme inactivation. On the contrary cinnamaldheyde, although less powerful than eugenol, can react and cross-link with DNA and proteins other than interact with cell membranes. Eventually, spices possess other degradation compounds originating from unsaturated fatty acids, lactones, terpenes, glycosides, and sulfur- and nitrogen-containing molecues. For instance, the mode of action of AITC, a nitrogen-containing compound, is generally considered as a non-specific inhibition of periplasmic or intracellular targets. In fact, due to its highly electrophile central carbon atom, it can inhibit enzymes and affect proteins by oxidative cleavage of disulfide bonds (Hyldgaard et al., 2012). AITC is the main constituent of mustard essential oil. Clemente et al. (2016) reported that mustard EO induced cell cycle arrest, resulting in bacterial filamentation.

Other than affecting membrane and intracellular stability, Szabo et al. (2010) reported that clove, oregano, lavender, and rosemary essential oils possess quorum sensing inhibitory activity. For instance, molecules such as furanones can be internalized by bacteria, bind to LuxR-type proteins, and destabilize them (Camilli and Bassler, 2006). In this way spices could impact the motility, swarming, and biofilm production of bacteria. Overall, antimicrobial activity of spices cannot be confirmed based only on the action of one compound. The final activity is a synergistic effect of more components.

Conclusion

Starting from the food preparation, spices can affect both food spoilage microorganisms (food preservation) and human pathogens (food safety) due to the antimicrobial and antifugal activity of their natural constituents. Spices are provided from natural herbs and plants and generally recognized as safe (GRAS) by the American Food and Drug Administration (FDA). However, the need of high amount of natural compounds represent the main limitation for effective performance against microorganisms. Mostly, their organoleptic characteristics may impact the results of in vitro and in vivo trials. For this reason, combinations of spices or their pure natural compounds, applied with or without additional technologies, represent a promising alternative to avoid this problem. Synergistic effects can lead to a reduction of both natural compounds used and treatment applied. In several cases, additive activities have been also reported. The study of spices, natural compounds, and novel combination technologies can be source of inspiration for developing novel or enhanced molecules acting against spoilage microorganisms.

Statements

Author contributions

DG: Data compilation, manuscript writing, DB: Data compilation, table formation, SP: Data compilation, manuscript writing, and formating, AT: Data compilation, manuscript writing, editing and formatting, and final approval.

Acknowledgments

We thank Prof. V. Craig Jordan (Father of Tamoxifen) for providing the facility to revise the manuscript. This research was supported by a grant from the Ministry of Education, Science and Technological Development of Serbia (Project No. 173029).

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Summary

Keywords

inflammatory diseases, spices, food preservation, disease prevention, antimicrobial

Citation

Gottardi D, Bukvicki D, Prasad S and Tyagi AK (2016) Beneficial Effects of Spices in Food Preservation and Safety. Front. Microbiol. 7:1394. doi: 10.3389/fmicb.2016.01394

Received

20 January 2016

Accepted

23 August 2016

Published

21 September 2016

Volume

7 - 2016

Edited by

Michael Gänzle, University of Alberta, Canada

Reviewed by

Carlos F. Torres, Autonomous University of Madrid, Spain; Chibundu Ngozi Ezekiel, Babcock University, Nigeria

Updates

Copyright

*Correspondence: Amit K. Tyagi ;

This article was submitted to Food Microbiology, a section of the journal Frontiers in Microbiology

Disclaimer

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

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