The Dr. Jekyll and Mr. Hyde aspect of cooking herbs and spices: the medicinal properties and potential for contamination.
Currently, the US is the largest importer of spices accounting for greater than 80% of the total supply. (1) Herbs are commonly used today and have been used for years during the preparation of meals to increase the palatability of dishes and act as flavor enhancers. The reason that herbs were originally used in the preparation of foods was for their antimicrobial activity to preserve the food and prevent the development of a foodborne infection. Some of the herbs utilized most often in the culinary arts that possess potent antimicrobial activity are oregano, rosemary, cinnamon, ginger and garlic. The phytochemical components within herbs have demonstrated bacteriostatic or bactericidal activity.
In addition to their antimicrobial properties, these herbs have immunostimulatory effects on the organism consuming them as well as antioxidant activity. Many of these herbs also produce synergistic effects when combined, which potentiates their efficacy. The collective attributes of these herbs make them viable for use in food preparation. However, it is important to note that the heating of herbs can adversely affect their medicinal properties.
Another consideration is that herbs are susceptible to bacterial contamination by acting as reservoirs, which are capable of initiating outbreaks of foodborne illnesses. The most common pathogens responsible for the foodborne illnesses linked to spices and herbs are Salmonella, Bacillus cereus and Listeria. Over the years, foodborne pathogen outbreaks from Escherichia coli, Listeria, Bacillus, Shigella, Yersinia and Campylobacter have declined, but the incidence of Salmonella infections has remained the same or have slightly increased. (2) Therefore, the majority of outbreaks and recalls have been associated with Salmonella. According to the Food and Drug Administration (FDA), between 1970 to 2003, there were 21 recalls involving 12 different spices. (3) During this period, in the US per capita consumption of spices has increased by 60%. Paprika (Capsicum species) was most predominately involved spice in these recalls, followed by sesame seeds (Sesamum orientale) and oregano (Origanum vulgare).
In this review, we will examine the antimicrobial, immunostimulatory and antioxidant properties of herbs. The effects of heat on the stability of the active constituents within herbs will be analyzed. However, on the opposite end of the spectrum, we will investigate the potential of spices and herbs to act as a source for the spread of foodborne illness.
Oregano contains volatile oils, flavonoids and caffeic acids. The volatile oil component of oregano is predominately carvacrol and thymol. Carvacrol and thymol are the source of its antimicrobial effects. (4) Oregano is a broad spectrum, medium strength bacteriostatic agent with minimal bactericidal activity. (5) It is postulated that oregano is bacteriostatic against 75-100% of bacteria. (6) Oregano's most potent bacteriostatic activity was demonstrated against Acinetobacter baumanii, Aeromonas sobria, Klebsiella pneumonia, Enterococcus faecalis, Pseudomonas. aeruginosa, Salmonella typhimurium, Salmonella enterica, Serratia marcescens. Streptococcus faecalis, Staphylococcus aureus, Vibrio parahaemolyticus, Micrococcus luteus, Salmonella Indiana, Listeria innocua, Bacillus subtilis, E. coli and Hafnia alvei and is only bactericidal against Proteus vulgrais. (4) The inhibitory effect of oregano has been shown to prevent the pathological activity of foodborne pathogens in poultry, red meat, fried meat, vacuum-packed pork, cod, red grouper, eggplant and dairy products. (7)
The effectiveness of oregano on prevention of food borne pathogens can be observed in a study performed by the University of Bomova. In this study, iceberg lettuce was inoculated with Salmonella and then washed with 500 ppm of oregano oil for 1, 5 or 10 minutes. The population of Salmonella was measured using colony forming units (CFU) and was found to be reduced by 1.3, 1.65 and 2.28 log cfu/g respectively. (8) It was postulated that washing vegetables with oregano is capable of drastically reducing the population of Salmonella in a dose dependent manner. In a similar study, oregano efficiently inhibited the growth of antibiotic-resistant S. enterica on lettuce at concentrations as low as 0.1% (9)
A second study analyzed the potency of different herbs against E. coli 0157:H7, which is a virulent strain capable of inducing hemorrhagic colitis that can be lethal. (10) In this study, disc diffusion assays using five essential oils were performed and the diameter of inhibition was evaluated. The most significant effects against E. coil were produced by oregano and thyme (Thymus vulgaris) demonstrating both bacteriostatic and bactericidal activity with zones of inhibitions of 24.3 mm and 25.7 mm respectively. The mean bactericidal concentration of oregano was 625 mcg compared to 1,250 mcg of thyme at 20[degrees]C. Oregano exerted its antimicrobial effects in less than one minute. (11) This study demonstrates the potency and efficacy of oregano oil against a potentially lethal food borne pathogen.
Another study examined the concomitant effects of oregano and rosemary (Rosemarinus officinalis) as well as their activity against synergistic bacteria Lactobacillus plantarum, rhamnosus, reuteri and salivarius. The disc diffusion method was used to measure the minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC). Seven hundred and fitly broiler chickens were treated with either 100 mg/kg of oregano or rosemary volatile oils or 50 mg/kg of both. Both oregano and rosemary produced inhibitory effects. However, rosemary was only bacteriostatic against E. coil, S. Indiana and L. innicua while oregano was more potent against all of those strains and S. aureas and B. subtilis in addition. (12) Oregano and rosemary also proved to be synergistic in nature. The combination group possessed higher degrees of inhibition against all strains except B. subtilis. (12) Oregano was still the most potent agent when administrated alone. The last aspect of the study demonstrated that none of the groups hindered the growth of Lactobacillus species. (12) The synergistic nature of these herbs as well as their potent individual effects are demonstrated in this study against pathogenic, but not symbiotic bacteria.
Rosemary contains caffeic acid, diterpenes, flavonoids, triterpenes and volatile oils. The antimicrobial attributes of rosemary are associated with its diterpene, caffeic acid and volatile oil content. The specific active constituents that are categorized as diterpenes, caffeic acids and volatile oils are carnosol, rosmarinic acid, camphene, camphor, bornylacetate, [alpha]-pinene and 1,8-cineole. (4) Rosemary is broad spectrum, medium strength antimicrobial agent (5) that is bacteriostatic against 75% of bacteria. (6) The inhibitory effects of rosemary have been observed against B. cereus and subtills, Clostridium botulinum, (7) S. aureus, Vibrio parahaemolyticus, Salmonella enteritidis, Indiana and typhimurium, L. innocua and monocytogenes, Campylobacter jejuni and E. coli. (5) Rosemary possesses protective effects against foodborne pathogenic contamination of red meat, liver, pork, sausage, poultry and dairy products. (7)
The protective effects of rosemary were revealed in a study conducted at the Federal Institute of Education using Aeromonas hydrophila. A. hydrophila is capable of causing gastroenteritis in humans who consume contaminated fish, water or minimally processed vegetables. (13) Both oregano and rosemary demonstrated a significant inhibition of bacterial activity 24 hours after exposure at 2.5 [micro]L/mL of oregano, 20 [micro]/mL, of rosemary and the combination of 0.625 [micro]L/mL of oregano and 5 [micro]L/L of rosemary. (14) The antibacterial effects were attributed to a reduction in the ability of the bacteria to utilize glucose and efflux cellular material simultaneously causing waste products to accumulate and depriving the bacteria of nutrients eventually contributing to cell death. (14) The disruption of these processes occurred immediately after addition of the essential oils. Physiological alteration of the plasma membrane of A. hydrophila was apparent after 6 hours. (14) This study exemplifies the ability of herbs to cooperate to eradicate pathogens.
Another experiment demonstrated the broad spectrum of antimicrobial activity that rosemary possesses against bacterial strains commonly associated with food spoilage and pathogenic infection upon consumption. Disc diffusion method was used to access the potency of rosemary. Rosemary essential oils were tested in an undiluted formula or with a 1:1 or a 1:2 ratio. The undiluted and the 1:1 ratio formulas produced the most powerful effects inhibiting the growth of 27 strains of bacteria while the 1:2 serial dilution prevented the growth of 22 strains of bacteria. The undiluted concentration of rosemary established a zone of inhibition greater than 10 mm for all 27 strains except P. aeruginosa and fluorescens and E. coli. The strains of bacteria most susceptible to the undiluted extract were Acinetobacter iwoffii and johnsonii, B. subtilis, Enterobacter cloacae, Erwinia carotovora, L. monocytogenes, Micrococcus luteus, S. enterica, S. thompson, Shigella flex/led and Yersinia enterocolitica. (15) The 1:1 ratio dilution generated a zone of inhibition greater than 10 mm in 17-27 strains of bacteria. (15) This study accentuates the fact that rosemary is not only an effective broad spectrum antibacterial agent against foodborne pathogen, but that it is potent as well.
In a study performed by the University of Edinburgh, the potency of essential oils were measured against E. coil, S. aureus, L. monocytogenes, S. enteritis and C jejuni. The bacteriostatic and bactericidal activity of 25 ILL of rosemary, cinnamon (Cinnamomum species), garlic (Allium sativum) and ginger (Zingiber officinale) were established using the agar well dilution technique. The mean values for the zone of inhibition for rosemary, cinnamon, garlic and ginger were 8.7 mm, 10.1 mm, 4 mm and 4.3 mm for E. coli, 5.9 mm, 7.5 mm, 4 mm and 4.5 mm for S. aureus, 7.1 mm, 6.8 mm, 4 mm and 4.3 mm for L. monocytogenes, 9.3 mm, 10.9 mm, 4 mm and 4.3 mm for S. enteritidis and 9.3 mm, 8.9 mm, 4.4 mm and 5.1 mm for C. jejuni respectively. (16)
This study further evaluated the concentrations of the essential oils necessary to produce antimicrobial effects. The bacteriostatic and bactericidal activity of rosemary was observed at a concentration of greater than 1% of the essential oil for E. coli and S. enteritidis. (16) En contrast to rosemary, cinnamon produced the most potent bacteriostatic and bactericidal activity for almost all strains except S. aureus, L. monocytogenes and C. jejtmi. (16) Cinnamon and rosemary both produced bacteriostatic effects at a concentration of 0.04% and 0.05% for S. aureus and C. jejuni respectively while rosemary was a more potent growth inhibitor of L. monocytogenes with a concentration of 0.02% compared to a concentration of cinnamon, which was 0.03%. (16) Cinnamon most efficiently suppressed the cell growth of E. coli and S. enteritidis at a concentration of 0.05% for both organisms. It was also the strongest bactericidal agent for all strains with concentrations of 0.1% for E. coli, 0.04% for S. aureus, 0.075% for L. monocytogenes and 0.1% for S. enteritidis. (16) In comparison, garlic and ginger demonstrated bacteriostatic and bactericidal activity against all strains at concentrations greater than 1% indicating that are larger concentration was warranted to prevent growth and induce apoptosis of the bacteria. This study postulates the cinnamon is the most potent bactericidal agent.
Cinnamon contains volatile oils, diterpenes, oligomeric proanthocyanidins and mucilages. The antibacterial components of cinnamon are the proanthocyanidins especially procyanidin B2, cinnaldehyde, thymol and eugenol. Cinnamon is classified as a strong, broad spectrum antibacterial agent. (5) Cinnamon is estimated to inhibit the growth of almost 90% of foodborne pathogens. (6) This herb possesses bacteriostatic and bactericidal effects against most Staphylcoceus species, E. coll. L. monocytogenes, S. enteritidis, S. anatum, S. typhimurium, C. jejuni, Brucella abortus, Enterobacter sakazkii, B. cereus, B. subtilis, P. aeruginosa and C. botulinum. (7) Cinnamon has been used in the food processing industry for the preservation of ground beef, yogurt, alfalfa seeds and fruit. (7)
The proposed mechanism associated with the antibacterial activity of cinnamon is its ability to inhibit bacterial acetyl coenzyme A (CoA) carboxylase, which catalyzes the first committed step of fatty acid synthesis. (17) The first step in this process is characterized by the carboxylation of biotin using adenosine triphosphate (ATP) to provide the driving force. Next the carboxyl group is transferred to the acetyl group producing malonyl-CoA. (18) Malonyl-CoA is the carbon donor responsible for elongation of the carbon chain during fatty acid synthesis. Inhibition of this enzyme prevents the synthesis of fatty acids, which can impede the growth of bacteria. (18)
A study conducted at the University of Hong Kong demonstrated the potency of cinnamon against B. cereus, L. monocytogenes, S. aureus, E. coli and S. anatum. The MIC and MBC of cinnamon were evaluated. Cinnamaldehyde and procyanidin B2 produced the largest zones of inhibition and had MIC values ranging from 125-500 mcg/mL and 78.1-2,500 mcg/mL respectively and MBC values ranging from 312.5-2,500 mcg/mL and 78.1-2,500 mcg/mL respectively. Cinnamaldehyde was the most potent bacteriostatic component against all forms of bacteria with zones of inhibition for B. cereus, L. monocytogenes, S. aureus, E. coli and S. anatum measuring 43.3 mm, 50.2 mm, 68.6 mm, 41.4 mm and 22.3 mm respectively. The zones of inhibition for procyanidin B2, the next most potent agent, were 21.4 m, 18.4 mm, 21.5 mm, 9.8 mm and 11.4 MM. (19) The constituents of cinnamon were found to have significant antibacterial properties prompting the investigators to propose that cinnamon would be an effective agent for the prevention of transmission of foodborne pathogens caused by contaminated food products. (19)
The next study evaluated the antibacterial effects of cinnamon and oregano against C. jejuni, which is the leading cause of bacterial diarrhea worldwide. (20) The bactericidal activity of the components carvacrol from oregano and cinnamaldehyde from cinnamon at concentrations of 0.5%, 1.5% and 3% were examined against antibiotic resistant and susceptible strains of C. jejuni. In this experiment, broiler chickens were inoculated with the C. jejuni and wrapped in apple-based edible films containing the different concentrations of either carvacrol or cinnamaldehyde and incubated for 72 hours at 4[degrees]C or 23[degrees]C. Cinnamaldehyde at concentrations of 1.5% and 3.0% reduced antibiotic resistance and susceptible strains of C. jejuni at 4[degrees]C by 0.2 and 2.5 logs and 1.8 and 6.0 logs respectively. At 23[degrees]C, the 3% carvacrol concentration disrupted the growth of both the C. jejuni sensitive and antibiotic resistance strains by 2.4 logs. Reductions for cinnamaldehyde were greater than carvacrol at 23[degrees] C. (20) The significant inhibitory effects of cinnamon and oregano on antibiotic resistant strains of C. jejuni demonstrates their wide range of efficacy.
Another study measured the zone of inhibition of cinnamon, garlic and ginger against B. cereus. E. coil and S. aureus. The different concentrations of each essential oil solution measured was 0.5%, 1%, 2% and 3%. Garlic was the most potent inhibitor of the growth of B. cereus at all concentrations with zones of inhibition at 11.6 mm, 12.6 mm, 14.0 mm and 14.3 mm respectively. (7) Cinnamon was next most powerful bacteriostatic agent at 10.3 mm, 11 mm, 11.3 mm and 12 mm respectively followed by ginger at 9.6 mm, 10.3 mm, 11 mm and 11.6 mm respectively. Although all solutions significantly inhibited E. coil, cinnamon was most potent with zones of inhibition measuring 8 mm, 10 mm, 12.3 mm and 14.3 mm respectively. The next most potent agent was garlic at 10 mm, 10 mm, 11.3 mm and 12.3 mm respectively and ginger with 9.3 mm, 10.3 mm, 10.6 mm and 11.3 mm respectively. (7) However, ginger hindered the growth of S. aureus to the highest degree with zones of inhibition at 10.6 mm, 11.3 mm, 13 mm and 14.6 mm respectively. Garlic was the second most effective agent preventing growth up to 10.6 mm, 11.3 mm, 12.3 mm and 14 mm respectively. The least bacteriostatic agent was cinnamon with zones of inhibition at concentrations of 2% and 3% measuring 10 mm and 11.6 trim. (7) The data presented in this study demonstrates the efficacy of cinnamon, garlic and ginger against common foodborne pathogens. Each of the herbs consistently inhibited the growth of the bacteria at all concentrations with high zones of inhibition. There was very little difference between the zones of inhibition indicating that each herb can effectively prevent microbial growth during food preparation and the transmission of bacteria leading to an infection.
Ginger is another effective antimicrobial agent. Ginger contains volatile oils, aryl alkanes, gingerols, shogaols, gingerdiols, diarylheptanoids and starch. The individual components that possess antibacterial activity are the zingiberene (21), gingerols and shogaols. (22) Ginger is considered to be a weak, medium spectrum antibacterial agent with bacteriostatic activity against about 30% of organisms. (6) The microorganisms that ginger has produced bacteriostatic effects against are B. cereus, E. coli, S. aureus, L. monocytogenes, S. enteritis, Micrococcus letueus (23), B. subtilis and C. jejuni. (4) Ginger is not used as a preservative for the preparation of packaged foods.
Although ginger is not used in the packaging and processing of food and is considered a weak antibacterial agent, this herb is capable of inhibiting the growth of many virulent foodborne pathogens. A study conducted evaluating the MIC of ginger and oregano and five other commonly used spices was performed. In this study, irradiated minced meat was inoculated with S. aureus, L. monocytogenes, E. coil and S. Enteritidis and essential oils and maintained for three hours. Serial dilutions and pour plates were prepared and incubated at 5[degrees]C for 3 to 24 hours and then the CFU was measured. Ginger demonstrated its most potent effects at 6 hours after inoculation and lowered the cfu/g by almost 1.5 units. However, at 24 hours the bacteria on the plate preserved by ginger increased by ~0.5 cfu/g. (24) Oregano demonstrated a moderate decrease in bacterial growth by about 1 unit after 6 hours and it steadily reduced just below ginger at 24 hours. (24) This study suggests that ginger possesses rapid and powerful antibacterial effects for a short period of time. Therefore, it can be postulated that ginger may be one of the most beneficial herbs to use for immediate prevention of antibacterial growth during food preparation while oregano may be advantageous to use for longer term preservation.
Another study, evaluating the strength of 21 different herbs found that ginger was the most potent bacteriostatic agents against C. jejuni, which is capable of adhering to the gastrointestinal (GI) tract causing an infection. There is evidence that C. jejuni is increasingly resistant to antibiotics. (25) Ginger prevented the adherence of half the population of C. jejuni to the mucosal wall of the GI tract and its growth at a concentration of less than 0.1 mg/mL. The next most bacteriostatic herb was cayenne (Capsicum annum) at a concentration of 29 mg/mL. (26) This study demonstrates that although ginger is considered a weak antibacterial agent overall, it can be a very effective agent against certain strains of bacteria. It should be noted that in this study ginger prevented the growth of C. jejuni to a higher degree than agrimony (Agrimonia euputoria), licorice (Glycerrhiza glabra) and andrographis (Andrographis paniculata). Agrimony is used predominately for the treatment of acute diarrhea (4) while licorice and andrographis are adaptogenic agents with both antibacterial and immunes system up-regulating activity. (4) The fact that ginger was more effective than these other highly regarded herbs demonstrates its efficacy.
Additional evidence that ginger is a more potent antibacterial agent than it is currently considered is revealed by its ability to eradicate antibiotic resistant bacteria. A study evaluating the activity of garlic and ginger against antibiotic resistant strains of E. coli, P. aeruginosa, B. subtilis, S. aureus, K. pneumonia, S. sonnei, S. epidermidis and S. typhi was performed. Disc dilution method was used to measure the efficacy of aqueous, ethanol and methanol extracts of garlic and ginger. The garlic aqueous extract overall exhibited the highest degree of bacteriostatic activity, yet the ethanol and methanol extracts of ginger also produced potent inhibitory effects. The aqueous extract of garlic produced a zone of inhibition against E. coil, P. aeruginosa, B. subtilis, Shigella, S. aureus, K. pneumonia, S. epidermidis and S. tiphi at 14.3 mm, 18.3 mm, 18.6 mm, 13 mm, 19.3 mm, 15.6 mm, 22 mm and 15.6 mm respectively. (27) The most pronounced effects of ginger ethanol extract were observed against E. coil, P. aeruginosa, B. subilliv and S. epidermidis with zones of inhibition at 15 mm, 14 mm, 13.6 mm and 15 mm. The methanol extract of ginger was most potent against S. aureus, K. pneumoniae and S. typhi with the inhibition of growth at 14.3 mm, 12 mm and 11.7 mm. The ethanol and methanol extracts both demonstrated equivalent levels of growth inhibition against Shigella at 15 mm. (27) Even though garlic generated the most bacteriostatic activity against the antibiotic resistant strains of bacteria, ginger demonstrated comparable inhibitory zones against most antibiotic resistant strains and was more effective against antibiotic resistant E. con and Shigella.
One of the most potent anti-bacterial agents is garlic. The primary constituent in garlic is alliin, which is converted to allicin by damaging the tissue of raw garlic cloves promoting the release of alliinase. Alliinase is an enzyme contained within vacuoles that catalyzes the conversion of alliin to allicin. Allicin is responsible for the medicinal effects of garlic. Garlic is considered to be a strong, broad spectrum bacteriostatic agent effective against 75-100% (6) of bacteria and is especially effective against a wide range of antibiotic resistant bacteria. (4) Garlic is bacteriostatic against Helicobacter pylori, Bacillus species, Escherichia species, Staphyloccus species, Streptococcus species, Pseudomonas species, Mycobacteria species, Enterococcus species, (4) Salmonella species, Shigella species, K. pneumonia, (27) V. parahaemolyticus, (7) L. monocytogenes, C. jujeni, (16) Vancomycin resistant enterococci, (4) multidrug resistant mycobacterium tuberculosis (28) and Streptomycin resistant S. aureus and E. coli. (29) Despite garlics powerful antibacterial activity, garlic is not commonly used for the preparation and preservation of packaged foods.
The antibacterial properties of garlic were assessed against the pandemic strain of V. parahaemolyticus, which is one of the leading causes of pathogenic GI disease in the US and accounts for half of food poisoning outbreaks in certain Asian countries. (30) The efficacy of garlic was determined using the disk diffusion method. Freshly squeezed garlic produced a zone of inhibition of 11.6 mm. (31) Due to the virulent nature of this bacterium, it is crucial to appropriately prepare food using an antibacterial agents such as garlic to prevent the transmission and spread of infections.
One of the studies demonstrating the efficacy of aqueous garlic extract was performed on 133 multidrug resistant gram positive and gram negative bacterial strains. The bacterial strains observed in this study were S. aureus, S. epidermidis, S. pneumonia, S. pyogenes, H. influenza, S. typhi, P. aeruginosa, E. coli, Shigella species and Proteus species. Bacteriostatic activity was evaluated using the disc diffusion and macrobroth dilution methods. The zones of inhibition for gram positive bacteria ranged from 20.2-22.7 mm and 19.8-24.5 mm for gram negative bacteria. (32) The MIC for garlic ranged from 14.3-15.6 mg/ml and 22.937.2 mg/ml for gram-positive and negative species respectively. (32) The strength and versatility of garlic are demonstrated in this study. It is not only an effective herb for preventing the growth of bacteria, but it demonstrated bacteriostatic activity against multidrug resistant strains.
A study was conducted using 148 extracts from 37 different types of fruit, vegetables, grains, herbs and spices. Both organic and aqueous extracts of garlic, black peppercorns (Piper nigrum), ginger, apple (Malus species), banana (Musa species) and orange (Citrus species) were used to treat food products. The effects that the different extracts had on the pathological and synergistic bacteria in the GI tract were examined. Garlic and black peppercorns significantly enhanced the growth of L. reuteri while simultaneously inhibiting the growth of the pathogenic bacteria E. coli 0157:1-17 and LF82. (33) Apple, banana and orange all inhibited the growth of both E. coil strains and enhanced the growth of L. reuteri, L. rhamnosus and Bifidobacteria lactis, which are all beneficial bacteria. Ginger significantly inhibited both pathogenic strains of E. coli and had no effect on the synergistic strains. (33) This study demonstrates that garlic is not just a potent antibacterial agent, but it enhances the growth of symbiotic bacteria. In contrast, ginger had no effect on the beneficial bacteria in the GI tract. However, it reduced the growth of the pathogenic bacteria, which may indirectly promote the growth of the normal flora.
Only one study reported the immune up-regulating activity of oregano. The study was conducted on growth-retarded, low weight pigs. Administration of the dried leaf and flower extract of the oregano contained 500 g/ kg of volatile oils. Pigs fed with the oregano supplement had significantly higher immunostimulatory response characterized by an increased production of cluster of differentiation (CD) 4 and CD8 T-cells, major histocompatibility complex (MHC) II and peripheral blood lymphocytes. (34)
CD4 and CD8 T-cells are coreceptors expressed on the surface of T-cells. CD8 coreceptors are on the surface of all T-cells and CD4 coreceptors are on the surface of T-helper cells. CD8 and CD4 strengthen the bond that is formed between MHC 1 and 11 respectively enhancing the activity of the T-cells and promoting a generalized immune response. (35) Both of these CD T-cells may also be present on macrophages and CD8 may be expressed on natural killer cells, mast cells and dendritic cells. (36) MHC cell II proteins are located on the surface of B-lymphocytes, macrophages and other antigen presenting cells and function to eradicate antigens and enhance the immune system function through the antigen presenting pathway. (35)
Rosemary has been shown to enhance the body's natural defenses. A study found that dosages of 10, 50 and 100 mg/kg of rosemary for eight weeks significantly enhanced the immune system in mice inoculated with sheep erythrocytes. The study showed that immunoglobulin M and G increased by 26.95%, 36.5% and 70.78% and 5.74%, 36.61% and 36.64% for 10, 50 and 100 mg/kg of rosemary respectively when compared to the control group. (37) The 100 mg/kg group was the only group that significantly increased mitogenic proliferation of T and B-lymphocytes over the control group. (37)
Some evidence suggests that cinnamon may enhance the natural immune defenses of the body. One study showed that cinnamon increased the activity of CD8 T-cells potentiating their cytotoxic activity. (38) Another study found that cinnamon inhibited anti-CD3 antibody activity and promotes the secretion of interleukin 2. (39) Anti-CD3 antibodies act as immunosuppressive agents while interleukin (IL) 2 is a critical component necessary for the growth, proliferation and differentiation of T-cells. (40), (41)
Ginger also has the ability to promote the activity of the immune system. Ginger can induce the release of both IL 1 and 6 and granulocyte-macrophage colony stimulating factor. IL 1 and 6 are both cytokines secreted in response to an acute bacterial infection to stimulate the immunes system to prepare to resist a pathogen. (42) The granulocyte-macrophage colony stimulating factor enhances the function of the immune system by potentiating the release of IL 1 and IL 2 promoting cellular communication and presentation of antigens to B-cells. (43) Ginger has been found to increase respiratory burst and phagocytic activity. (44) Respiratory burst is the process of granulocytes phagocytizing antigens and denaturing them utilizing reactive oxygen species.
Garlic possesses potent immune system augmenting effects as well. Garlic has been shown to increase T-cell proliferation and natural killer cell activity in human subjects. In a study, subjects were administered an aged garlic extract for 90 days. After 45 days, subjects consuming garlic experienced a significant increase in T-cell proliferation and natural killer cell activity. (45) Garlic supplementation did not prevent infection, but the incidence, severity and duration of illnesses reported were reduced 58%, 21% and 61% respectively. (45)
Garlic has the ability to stimulate splenocyte and thymocyte proliferation and up-regulate the expression of IL-2 and interferon-[gamma]. The spleen is the largest lymphatic organ in the human body and participates in lymphocyte proliferation, immune surveillance and initiation of the immune response. (46) The thymus is another lymphatic organ, but is more active during childhood and begins to diminish after puberty. However, it continues to produce lymphocytes to assist with maintenance of the immune system. (46) Interferon-[gamma] is a cytokine that is secreted to activate macrophages and nonspecific phagocytes. (35) Accordingly, other studies have shown that garlic increases phagocytic activity (47) and the production of reactive oxygen species through the process of respiratory burst within macrophages. (48) Macrophages have also been reported to have a higher degree of microbicidal activity in individuals consuming garlic. (46)
The antioxidant effect of herbs is another important consideration that is positively correlated with immune health. High levels of oxidative stress are associated with illnesses caused by both viral and bacterial pathogens. (49) Myeloperoxidase is an enzyme that is contained within white blood cells. This enzyme utilizes hydrogen peroxide within the vacuole of a cell to produce hypocholorous acid, which is a strong toxin. (50) During phagocytosis, hypochlorous acid is used to denature antigens such as bacteria and viruses. Unfortunately, during this process a free radical known as superoxide is released. (50) Superoxide radicals are not very powerful and can only diffuse a short distance. However, a significant amount of superoxide can be generated with the high degree of phagocytic activity present during an illness increasing the levels of oxidative stress and potentially being converted to hydrogen peroxide, which is a more reactive and destructive oxygen species. (50)
Hydrogen peroxide can in turn engender hydroxyl radicals, which are the most potent and destructive radicals capable of damaging DNA, proteins or membranes. (50) These high levels of oxidative stress can rapidly deplete the natural antioxidants within the body. (50) Therefore, herbs and spices with antioxidant activity are essential for preventing the rise of free radicals and depletion of antioxidants.
Oregano is a potent antioxidant. One study found that oregano was a more powerful antioxidant agent against superoxide induced lipid peroxidation than ascorbic acid. Ascorbic acid or vitamin C is one or the most powerful water soluble antioxidants. Oregano was also capable of reducing the levels of other reactive oxygen species and it enhanced the activity of glutathione, which is another powerful antioxidant that converts hydrogen peroxide into two water molecules. (51)
Rosemary contains phenolic compounds, flavonoids and caffeic acid capable of producing antioxidant effects. In a study, rosemary was capable of significantly reducing the levels of lipid peroxidation. (52) The herb potentiated the antioxidant effects of glutathione, superoxide dismutase and catalase. (52) Superoxide dismutase converts superoxide radicals into oxygen and hydrogen peroxide and catalase converts hydrogen peroxide into water and oxygen."
The antioxidant activity of cinnamon varies depending on the species that is being used within the extract. Cinnamomum zeylanicum bark demonstrated a reduction in lipid peroxidation and increased levels of reduced glutathione, glutathione peroxidase and catalase (53) Cinnamomum cassia has been found to be rich in flavonoids and polyphenols. The total polyphenolic content ranged from 0.151-2.018 g/100 g. (54) This is an average number of polyphenols when compared to a known potent source of antioxidants such as grape based red wine, which contains 5.5 g/100 g of polyphenols. (55) Cinnamomum verum is not noted for its antioxidant activity. (4)
Ginger contains anthocyan in, flavonoids and isoflavonoids capable of producing antioxidant effects. (56) Ginger is capable of reducing lipid peroxidation. (4) Studies have found that 6-shogaol found within ginger was capable of inducing the antioxidant response element pathway effecting nuclear transcription factors and increasing their activity. As a result, superoxide dismutase, glutathione peroxidase and catalase activity were all elevated. (57)
Garlic has the capacity to reduce oxidative stress experienced in individuals suffering from cardiovascular disease. (4) A study revealed that components of garlic such as S-allyl cysteine are able to prevent the generation of reactive oxygen species (58) by perpetuating the function of the mitochondria during oxidative phosphorylation (59) or through the modulation of neuronal nitric oxide synthase activity. (60) Oxidative phosphorylation generates superoxide radicals while nitric oxide synthase produces nitric oxide, which is capable of acting as a reactive oxygen species. Potentiation of glutathione-S-transferase, glutathione peroxidase, superoxide dismutase and catalase activity (59) and mRNA expression has also been observed. (61) Garlic can prevent oxidative damage to proteins, lipids (59) and DNA. (62)
The addition of different herbs and spices to meals for medicinal purposes has become a common practice in many cultures. However, evidence exists suggesting that although these spices are acting as flavor enhancers, many of the active constituents that possess healing properties are not being released or are destroyed during food preparation. As mentioned above, garlic is bacteriostatic and has the ability to act as an immunostimulatory agent. The active component within garlic is allicin, which is formed from allicin by damaging the tissue of raw garlic cloves. (4) Therefore, to achieve optimal therapeutic effects of allicin, the raw garlic used in food preparation must be cleaved or crushed.
The second consideration is the effect that heating herbs and spices have on their nutrient content. Heating these components can damage or destroy them negating there potential beneficial effects. One study evaluated the medicinal value of cooking crushed versus cooking whole garlic. The results showed that the uncrushed garlic was slightly more effective than crushed garlic when heated for 3 minutes at 200[degrees] C, yet both forms of garlic still produced similar levels of activity when compared to raw garlic. (63) However, when the herb was heated for 6 minutes, the activity of uncrushed garlic was inhibited while the crushed garlic still demonstrated a quarter of its original strength. (63) The allicin content was also evaluated. The concentration of allicin in uncrushed garlic was less than 6% after 6 minutes while the allicin content of crushed garlic gradually decreased reaching levels comparable to uncrushed garlic at 20 minutes. (63) Similar effects were observed with the boiling of garlic. However, concentrations of allicin in both forms were diminished after 10 minutes. The study also showed that microwaving garlic prevented its therapeutic activity whether crushed or uncrushed. However, the addition of garlic juice to crushed samples increased its medicinal value. (63)
Another study conducted with extracts of cinnamon, cloves (Syzygium aromatieum), fennel (Focnieulum vulgare), ginger, lavender (Lavandula angustifolia), parsley (Petroselinum crispum), rose (Rosa canina), rosemary, sage (Salvia officinalis) and thyme measured the antioxidant activity before and after cooking. This study found that simmering or adding the herbs to soups greatly increased antioxidant potential while stir frying and grilling the herbs reduced their activity. (64) Based upon these results and the results of the previous study, it can be postulated that cooking herbs and spices at lower temperatures may either enhance or minimally affect the medicinal values whereas cooking herbs and spices for long durations at high temperatures can drastically impair the activity and content of the medicinal components.
Food borne Pathogens Associated with Spices
According to Center of Disease Control (CDC), each year roughly 1 in 6 Americans (or 48 million people) succumb to an illness, 128,000 are hospitalized, and 3,000 die of foodborne diseases. (65) Bacterial pathogens predominate in foodborne illnesses while Noroviruses and other enteric viruses can cause foodborne outbreaks as well. Four of the top five foodborne pathogens in the US are bacteria. S. enterica and a variety of its serotypes including enteritidis are most commonly associated with foodborne illness. Salmonellosis presents as mainly diarrhea and accompanying dehydration. In vulnerable hosts, however, Salmonella can cause more serious infections. Each year about 40,000 cases of acute salmonellosis are reported to the CDC, but since milder infections may not be reported the total infections every year are estimated to be thirty times higher. Salmonella is responsible for 400 deaths every year. (66)
Another foodborne pathogen, E. coli O157:H7 is more likely to be associated with meat and with greater surveillance we have seen a decline in infections with this pathogen. E. coli O157:147 is notorious for causing severe bloody diarrhea and in vulnerable hosts, especially children, and can cause hemolytic uremic syndrome with fatal consequences. L. monocytogenes is known for causing foodborne illness linked to refrigerated foods. L. monoclvtogenes not only survives in the cold, but actually thrives at these temperatures. Thus contamination with this pathogen in ready to eat foods, fruits and other cold food preparations is a major concern. In addition, this pathogen is known to form biofilms on food processing surfaces. Biofilms make it difficult to get rid of Listeria from the food processing surfaces unless stringent disinfection procedures are followed.
Spore bearing pathogens such as B. cereus and Clostridium perfringens typically cause toxin mediated emetic (vomiting) or diarrheal illness due to release of enterotoxins in the food. Subsequent heating of the food does not destroy these toxins. Hence these pathogens are especially critical in ready-to-eat meals, which are mostly heated in the microwave or at low temperatures. Spores will survive most of the decontamination procedures used for rendering the food safe. B. cereus produces two types of toxins, a heat stable toxin that gives rise to diarrheal illness and a heat labile toxin, which leads to nausea and vomiting. B. cereus is an aerobic bacillus. It can readily germinate in presence of oxygen and carbohydrates. Rice is a very conducive medium. Hence if B. cereus is introduced into the cooked rice it can allow the spores to germinate and produce toxins. One of the spices added to rice in many recipes is cumin (Cuminum cyminum). Cumin seeds are dried, but if they are contaminated with the spores of B. cereus, the spores will readily survive desiccation as well as cooking temperatures. There have been many outbreaks and recalls related to contamination of cumin seeds with B. cereus. The contamination levels tend to be the highest in ground cumin seeds. (67)
Foodborne illness within the US is most commonly caused by contamination of the food at the source. In the last few years, there has been a decline in many of the common pathogens such as Listeria, Campylobacter and E. coli 0157:H7, but the incidence of Salmonella infections has remained almost the same or slightly increased. (2) Ills often very difficult to trace the exact ingredient which is contaminated as there are many ingredients in a given food recipe. In the last several decades, the US has increased its spices' consumption by nearly 60%, as the American palate has expanded to include a variety of ethnic as well as local foods. Eighty percent of these spices are imported from all over the world and not regulated or controlled by U.S. Department of Agriculture (USDA). Many ethnic preparations use a mixture of spices and herbs. Many of the dishes that use spices are meat based recipes and hence the introduction of potential pathogens further compounds the problem, providing a rich food source for the pathogens to grow. However, vegetarian recipes can be vulnerable to bacterial contamination with the use of spices as well. Interestingly many foodborne outbreaks have been linked to spices. It is easier to determine the potential danger of introducing pathogens by analyzing the contamination at the source of spices rather than trying to isolate it in the recipes.
In a recent study by Van Doren et al, Salmonella prevalence in spice shipments to the US during 2007-2009 was 0.066 (187 positive samples out of 2,844 examined) (1) A variety of serotypes have been reported. Salmonella is relatively resistant to drying and can survive for long periods of time on dried foods. In addition, Salmonella invades the inner tissues of the leaves and some fruits and thus resists surface sterilization. (68) In 2007, a significant outbreak was linked to Veggie Booty. Another outbreak that occurred in 2009-2010 involved 272 cases and was traced to products made with black and red peppers (Capsicum species) (69) It is important to realize that many smaller outbreaks that involve a few cases may never be reported to CDC. The actual problem of spice mediated foodborne illness may be greater than we know. Peppercorns and paprika are especially notorious for being contaminated with Salmonella, but many other spices have been implicated as well. According to the FDA, during 1969 to 2003, there were 21 recalls involving 12 spice types. In this study by FDA, the majority of spices were powdered or ground including paprika, black pepper, oregano, cumin, sage, thyme etc. The leaves of basil (Ocimum basilicum) and bay (Laurus nobilis) as well as sesame seeds were implicated in the rest. (3) Ground spices in general have a greater pathogen load, however, there are some studies which have demonstrated no difference in the pathogen loads. Plant leaves that are used as herbs/spices also have higher degree of contamination, for example cilantro (Coriander sativum), fresh basil, herbal teas. (70)
Selected foodborne outbreaks in recent years traced to spices in the LS. Year Pathogen Source Number of Reference cases 2009-2010 Salmonella Black and 272 69 Montevideo red pepper 2008 Salmonella Jalapeno 1500 73 Saintpaul peppers (capsicum) 2007 Salmonella White 87 74 Rissen pepper
Since the spice trade and usage is worldwide, many countries are investigating outbreaks and recalls due to spice contamination. Sagoo et al have reported the prevalence of Salmonella as 1.5 and 1.1% in spices and herbs respectively with overall 3.0% incidence of B. cereus, C. perfringens and E. coli. (71) Hara-Kudo et al reported in 2006 that black and red pepper were contaminated with Salmonella in spices imported to Japan, (72) it follows that steps must be taken to reduce the potential pathogen load in spices and herbs in both fresh as well as dried varieties.
Approaches to Decreasing the Contamination of Spices from Farm to Fork
Since a majority of contamination occurs before the spices are harvested or processed, it is important to prevent exposure of spices and herbs to the sources of microorganisms. The known sources of Salmonella are animals including poultry birds. Restricting access of the animals including poultry birds to areas or the soil used for growing spices is very important. In addition we must realize that animal manure or organic compost used as a fertilizer can serve as a source of pathogens as well. There have been a few studies that have explored the effect of composting on the pathogen's survival or inactivation. (75) Guidelines in composting for fertilizers for human food productions need to take into account the potential for fecal contamination from domestic and wild animals. The processes also need to address contamination by pathogens such as E. coil, Listeria and Salmonella, which are vegetative cells versus spore bearers such as B. cereus and C. perfringens.
Enteric bacteria such as Salmonella and E. coli have variable susceptibility to drying, but are generally vulnerable to temperatures above 55[degrees]C maintained for at least 3 days. However, the spore bearers are not destroyed at this temperature. To destroy the spores, temperatures of 120[degrees]C are required. At such a high temperature, the taste and properties of the spices and herbs are going to be significantly impacted. One of the important measures to prevent the bacterial load or presence of pathogenic bacteria in the fertilizers of foods that are likely to be eaten raw is to choose the raw material for compost carefully. The herbs that are consumed raw include fresh cilantro, fresh parsley, oregano etc. Care must be taken not to mix domestic or nongrazing farmland waste with grazed land waste during composting. Most people are not even aware of the source for the organic compost that they are buying to grow their own herbs and spices in. It is also very important for people who make their own compost from the vegetable and other waste material from their household to prevent access of wild or domestic animals including poultry to the compost site.
The water used for irrigation is another source of these potential pathogens. While the concentration of the pathogens may be very low in the water used for spray irrigation, the persistence of Salmonella on the plants in significant quantity has been demonstrated in fresh herbs such as Parsley. (68) Many of these herbs are used in the recipes as garnishing and not cooked at all. The organisms tend to persist in the leaves and stalks for many days post irrigation.
Food Decontamination Procedures
Since the outbreaks associated with spices have been reported more recently there has been a move in the food industry to decontaminate the spices, especially dry spices when they are marketed. A variety of methods have been used for decontamination of spices and herbs. Traditionally many microorganisms such as fungi die as a result of desiccation, hence herbs and spices were dried. This process increased their shelf life, however, as we have realized, many common pathogens such Salmonella and spore bearers survived desiccation. Hence more aggressive methods have been adopted. Large commercial manufacturers of spices have used two common modalities for decontamination of spices including the gaseous methods such as ethylene dioxide and irradiation of food with gamma irradiation.
Irradiation has been used since the 1990s for decontamination of spices and seasonings. Irradiation of food commonly uses Cobalt 60 as the radionuclide as the source of gamma rays. The radiation dose limit for spices and seasoning (30 kilograys) as set by the US FDA is considerably higher than that approved for other foods such as fruit (1 kilograys) and poultry (3 kilograys). (76) Though, most manufacturers use much lower doses, typically up to 10 kilograys. The foods are not changed in nutritional value and they are not made dangerous as a result of the irradiation. The high energy ray is absorbed as it passes through food, and gives up its energy. The food is slightly warmed. If the food still has living cells, (such as seeds, or shellfish, or potatoes) they will be damaged or killed just as microbes are. This can be a useful effect. For example, it can be used to prolong the shelf life of potatoes by keeping them from sprouting. The energy can induce a few other changes. Horvothova, Suhaj and Polovka (77) demonstrated that at 5 to 30 kilograys black pepper, oregano and allspice (Pimento diocica) changed in color only temporarily. Brandstetter et al (78) observed that at 10 kilograys doses antioxidative properties of sage, thyme and oregano were not affected. Calcucci et al, however, did show a significant loss of ascorbate in black pepper, cinnamon, nutmeg (Myristica fragrans), oregano and sage. The carotenoids were also decreased in cinnamon, oregano, parsley, rosemary, bird pepper (Capsicum frutescens) and sage (79) Farkas has reviewed a variety of studies on irradiation at lower doses and comments that microorganisms treated with radiation with doses as low as 0.15-0.7 kilograys are more susceptible to environmental stresses and food processing treatments. (80) The lowest possible doses to destroy the spores can be applied to minimize the loss of ascorbate or carotenoids.
Irradiated foods need to be stored, handled and cooked in the same way as unirradiated foods. The rules of basic food safety must be followed during processing after irradiation to avoid recontamination because the irradiated foods have fewer microbes of all sorts including those that cause spoilage. They may have a longer shelf life before spoiling. The safety of irradiated foods has been studied in animals and people. According to CDC, (81) extensive well-controlled trials utilizing animal feeding studies lasting for multiple generations in several different species, including mice, rats, and dogs, showed there is no evidence of adverse health effects. In addition, NASA astronauts eat foods that have been irradiated to the point of sterilization (substantially higher levels of treatment than those approved for general use) when they fly in space. The safety of irradiated foods has been endorsed by the World Health Organization (WHO), the CDC and by the Assistant Secretary of Health, as well as by the USDA and the FDA. (82)
Newer technologies in irradiation methodologies include electronic beam technology (e-beam) and X-rays. Both have been demonstrated to be effective, but are used less commonly. An older and more established, although more intrusive, method is gaseous method using ethylene dioxide. This method has been used since the 1960s. It is cheaper than gamma irradiation, but must be done effectively. It requires complete penetration of the spices and herbs to be decontaminated and must be aerated adequately, usually for 24 hours, to remove the residue and the odor. It also approved for spice blends except those that contain salt. The presence of salt reduces its effectiveness. (82)
The use of certain herbs such as oregano, rosemary and cinnamon for the preservation of food products has been effective for the prevention of contamination by microbes. However, the addition of these herbs as well as garlic and ginger to meals during preparation can be equally effective for their broad spectrum bacteriostatic effects. As demonstrated in the previous studies, ginger produced potent inhibitory agent for short-term prevention of bacterial growth while the addition of oregano would be more advantageous for its long-term bacteriostatic activity. All of these herbs are capable of inhibiting the growth of Bacillus species, Escherichia species, Staphylococcus species, Salmonella species, Listeria species and campylobacter species, which are the most common perpetrators of food borne pathogenic outbreaks. The synergistic effects of rosemary and oregano have been demonstrated to enhance their bacteriostatic properties.
Another important consideration is that many of the herbs are effective against antibiotic resistant strains of bacteria. The number of antibiotic resistant strains of bacteria is on the rise in the US. Finding agents that are capable of inhibiting their growth and preventing debilitating or life-threatening infections is essential. Another characteristic of antibiotics is that they have the potential to eradicate the normal flower in the GI tract. Garlic, oregano, rosemary and ginger have been shown to have either no effect or promote the growth of symbiotic bacteria preventing adverse effects associated with the GI tract.
In addition, herbs have immunostimulatory and antioxidant effects. Although some herbs are more potent than others, oregano, rosemary, cinnamon, ginger and garlic all promote T-cell differentiation and have other effects to enhance the overall immune function. The positive attributes and immune enhancing potential are demonstrated in several studies. This suggests that not only are these herbs bacteriostatic and bactericidal, but they may prevent transmission of the pathogen by increasing immunoglobulins and lymphocytes. Although lymphocytes are primarily associated with viral infections, lymphocytosis can be involved with the immune response to acute bacterial infections as well. (83) Oregano enhanced dendritic cell activity, which can promote the growth of symbiotic bacteria while eliminating pathogens. (84) The ability of herbs to enhance antioxidant activity is essential due to the high levels of oxidative stress observed during and illness. Therefore, these herbs have the ability to enhance the degradation of bacteria and promote the natural defenses of the body to eliminate the foodborne pathogens.
Another way of inhibiting bacterial growth is through cooking. Cooking with spices and herbs is recommended for their medicinal value and prevention of bacterial contamination. However, the style of heating the herbs needs to be taken into consideration. Stir frying, grilling or cooking in the microwave can destroy the therapeutic properties of herb rendering them inactive. The addition of herbal components during the final few minutes of meal preparation or cooking at low temperatures can conserve their active components.
As we see, foodborne illness in the US is most commonly caused by contamination of the food at the source. Spices present are yet another source of these pathogens. Imported spices with very little regulatory oversight at the source of growing, harvesting and processing present a potential hazard. We have reviewed many outbreaks traced back to spices. The major pathogen involved is Salmonella, but other bacterial pathogens such B. cereus and C. perfringens also deserve attention due their ability to form spores. These spores can readily survive many traditional processing methods such as drying and heating.
The most reliable methods to eradicate these pathogens are ethylene dioxide and gamma irradiation. Safety of these methods has been demonstrated in several studies. Commonly contaminated spices are peppers of every kind and leafy herbs. Educating powers, harvesters and processors of methods to minimize the contamination from known sources such as animals is extremely important. Special attention must be paid to the herbs that are used as garnishing such as parsley, oregano and cilantro leaves. Thus spices are very important in all the recipes that we enjoy, but we must pay attention to their potential to cause foodborne illness and take appropriate precautions.
In conclusion, spices are a viable means of enhancing the preservation of food products with their antimicrobial properties. Garlic, rosemary, oregano, cinnamon and ginger are some of the most commonly used agents with potent antimicrobial activity. These herbs further offer benefits to the host through their immunostimulatory and antioxidant activities, which may reduce susceptibility to foodborne illness. However, some spices such as black and red pepper or fresh cilantro, parsley and oregano are vulnerable to contamination by foodborne pathogens. Hence, care must be taken to avoid contamination from farm to fork by avoiding contact with reservoirs, inactivation during processing and safe handling of these spices. Educating spice and herb growers, processors and consumers as well as the newer decontamination technologies available such as gamma-irradiation will play a crucial role in prevention of hazardous foodborne pathogenic contamination associated with spices and herbs. It is important to note that cooking can reduce the number of antimicrobials on food, but it can also inhibit the medicinal activity of the herbs and spices. It is the recommendation of the authors to add herbs and spices to a meal within the last three minutes of cooking and avoid frying, grilling and microwaving to prevent denaturing of the therapeutic contents. It is imperative that every measure is taken to eliminate contamination of herbs and spices, since cooking cannot be relied upon to kill the foodborne pathogens.
(1.) Van Doren J.M. Kleinmeier D. Hammack T.S. Westerman A. . Prevalience, serotype diversity, and Antimicrobial resistance of Salmonella in imported shipment of spice offered for entry to the United States, FY 2007-FY2009. Food Microbiology.
(2.) Centers for Disease Control. . Vital Signs: Incidence and Trends of Infection with Pathogens Transmitted Commonly Through Food---Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 1996-2010. Accessed at the URL: http://www.cdc.gov/mmwr/preview/mmwrhtml/mm6022a5.htm?s_cid=mm6022a5_w
(3.) Vij V. Ailes E. Wolyniak C. Angulo F.J. Klonz K.C. . Recalls of Spices due to bacterial contamination monitored by the U.S. Food and Drug Administration: The predominance of Salmonellae, J Food Prot.
(4.)  Physician's Desk Reference for Herbal Medicine 4th Ed. Thomson: Montvale.
(5.) Synder, P. . Antimicrobial Effects of Spices and Herbs. Hospitality Institute of Technology and Management.
(6.) Billing J. Sherman P. . Darwinian Gastronomy: Why We Use Spices. BioScience.
(7.) Cliver D. Ibrahim S. Tajkarimi M. . Antimicrobial Herb and Spice Compounds in Food. Elsevier.
(8.) Gonul S. Gunduz G. Karapinar M. . Antimicrobial Activity of Oregano Oil on Iceberg Lettuce with Different Attachment Conditions, Journal of Food Science.
(9.) Friedman M. Gerber C. Jaroni D. . Antimicrobial Activity of Oregano Oil Against Antibiotic-Resistant Salmonella Enterica on Organic Leafy Greens at Varying Exposure Times and Storage Temperatures. Food Microbiology.
(10.) Blattner F. Boutin A. Davis N.  Genome Sequence of Enterohaemorrhagic Escherichia coli 0157:H7. Nature.
(11.) Burt S. Reinders R. . Antibacterial activity of selected plant essential oils against Escherichia coli 0157:H7. Letters in Applied Microbiology.
(12.) Bergaoui R. Bouzaienne T. Hamdi M. . Use of Rosemary, Oregano and a Commercial, Blend of Essential Oils in Broiler Chickens: in Vitro Antimicrobial Activities and Effects on Growth Performance. Journal of Animal Science.
(13.) US Food and Drug Administration. . Bad Bug Book: Foodborne Pathogenic Microorganisms and Natural Toxins Handbook Aeromonas hycirophila. Accessed at the URL: http://www.fda.gov/Food/FoodbornellInessContaminants/CausesofIllnessBadBugBook/ucm070523.htm.
(14.) Azeredo G. Figueiredo R. Souza E. . The Cytotoxic Effect of Essential Oils from Origanum vulgare L. and/or Rosmarinus officinalis L. on Aeromonas hydrophila. Foodborne Pathogens and Disease.
(15.) Mangena T. Muyima N. . Comparative Evaluation of the Antimicrobial Activities of Essential Oils of Artemisia afra, Pteronia incana and Rosmarinus officinalis on Selected Bacteria and Yeast Strains. Letters in Applied Microbiology.
(16.) Fyfe L. Smith-Palmer A. Stewart J. . Antimicrobial Properties of Plant Essential Oils and Essences Against Five Important Food-borne Pathogens. Letters in Applied Microbiology.
(17.) Gibbons S. Gilman S. Henken R. . Constituents of Cinnamon Inhibit Bacterial Acetyl CoA Carboxylase. Planta Medica.
(18.) Endermann R. Freiberg C. Habich D. . Novel Bacterial Acetyl Coenzyme A Carboxylase Inhibitors with Antibiotic Efficacy In Vivo. Antimicrobial Agents and Chemotherapy.
(19.) Brooks J. Cal Y. Corke H. . Antibacterial Properties and Major Bioactive Components of Cinnamon Stick (Cinnamomum burmannii): Activity Against Foodborne Pathogenic Bacteria. Journal of Agriculture and Food Chemistry.
(20.) Friedman M. Joens L. Law B. . Antimicrobial Edible Apple Films Inactivate Antibiotic Resistant and Susceptible Campylobacter jejuni Strains on Chicken Breast. Journal of Food Science.
(21.) Kerdchoechuen O. Laohakunjit N. Norajit K. . Antibacterial Effect of Five Zingiberaceae Essential Oils. Molecules.
(22.) Chen H. Chen Y. Chien H. . Zingiver officinale (Ginger.) Compounds have Tetracycline-Resistance Modifying Effects Against Clinical Extensively Drug-Resistant Acinetobacter Baumannii. Phytotherapy Research.
(23.) Chang M. Chang T. Chen H. . Antibacterial Properties of Some Spice Plants Before and After Heat Treatment. Zhonghua Min Guo Wei Sheng Wu Ji Mian Yi Xue Za Zhi.
(24.) Barbosa L. Fernandes A. Fernandes A Jr. . Essential Oils Against Foodborne Pathogens and Spoilage Bacteria in Minced Meat. Foodborne Pathogens and Disease.
(25.) Bone K. Cwikla C. Lehmann R. . Investigations into the Antibacterial Activities of Phytotherapeutics Against Helicobacter pylori and Campylobacter jejuni. Phytotherapy Research.
(26.) Bensch K. Bone K. Lehmann R. . Investigations into the antiadhesive activity of herbal extracts against Campylobacter jejuni. Phytotherapy Research.
(27.) Aslam S. Athar A. Gull I. . Inhibitory effect of Allium sativum and Zingiber officinale extracts on clinically important drug resistant pathogenic bacteria. Annals of Clinical Microbiology and Antimicrobials.
(28.) Absar M. lkram Ullah M. Javed K. . Antimycobacterial Activity of Garlic (Allium sativum.) Against Multi-Drug Resistant and Non-Multi-Drug Resistant Mycobacterium tuberculosis. Pakistan Journal of Pharmaceutical Science.
(29.) Ahmen M. Das S. Palaksha M. . Antibacterial Activity of Garlic Extract on Streptomycin-Resistant Staphylococcus aureus and Escherichia coli Solely and in Synergism with Streptomycin, Journal of Natural Science. Biology and Medicine.
(30.) Carrera-Flores D. DePaola A. Ishibashi M. . Pandemic Vibrio parahaemolyticus 03:K6, Europe. Center of Disease Control.
(31.) Bhoopong P. Hayeebilan F. Subhadhirasakul S. . Inhibitory Activity of Thai Condiments on Pandemic Strain of Vibrio parahaemolyticus. Food Microbiology.
(32.) Bamiro S. lwalokun B. Jimi-Otnojola J. . In Vitro Antimicrobial Properties of Aqueous Garlic Extract Against Multidrug-Resistant Bacteria and Candida Species from Nigeria. Journal of Medicinal Food.
(33.) Devoy S. Hedderley D. Lauren D. . In Vitro Effects of Food Extracts on Selected Probiotic and Pathogenic Bacteria. International Journal of Food Sciences and Nutrition.
(34.) Bilkei G. Walter B. . Immunostimulatory Effect of Dietary Oregano Etheric Oils on Lymphocytes from Growth-Retarded, Low-Weight Growing-Finishing Pigs and Productivity. Tijdschr Voor Diergeneeskunde.
(35.) Madigan M. Martinko J. Parker J. . Brock Biology of Microorganisms. Prentice Hall: Upper Saddle River.
(36.) Baba T. Ikeda H. Iwasaki S. . CD4+/CD8+ Macrophages Infiltrating at inflammatory Sites: a Population of Monocytes/Macrophages with a Cytotoxic Phenotype. Blood.
(37.) Abuharfeil N. Al Sheyab F. Bani Hani R. . The Effect of Rosemary (Rosmarinus officinalis. L.) Plant Extracts on the Immune Response and Lipid Profile in Mice. Journal of Biology and Life Science.
(38.) Im S. Hwang J. Jeon W. . Cinnamon Extract Suppresses Tumor Progression by Modulating Angiogenesis and the Effector Function of CD8+ T cells. Cancer Letters.
(39.) Cho D. Kang H. Kim Y. . Immunomodulatory Effect of Water Extract of Cinnamon on Anti-CD3-1nduced Cytokine Responses and p38, JNK, ERK 1/2 and STAT4 Activation. Immunopharmacology and Immunotoxicology.
(40.) Bach J. Chatenoud L. Primo J. . Anti-CD3 Antibody Induces Long-Term Remission of Overt Autoimmunity in Nonobese Diabetic Mice. Proceedings of the National Academy of Sciences of the United States of America.
(41.) Cantrell D. Smith K. . The Interleukin-2 T-Cell System: A New Cell Growth Model. Science.
(42.) Aud D. Dalrymple S. Krishna. . Interleukin-6 is Required for a Protective Immune Response to Systemic Escherichia coli Infection. Infection and Immunity.
(43.) Alpert A. Bressler L. Gillis S. . Granulocyte-Macrophage Colony-Stimulating Factor Augments the Primary Antibody Response by Enhancing the Function of Antigen-Presenting Cells. Journal of Immunology.
(44.) Chang Y. Chiang C. Hsieh S. . Dietary Administration of Zingerone to Enhance Growth, Non-Specific Immune Response and Resistance to Vibrio alginolyticus in Pacific White Shrimp (Litopenaeus vannamei.) Juveniles. Fish and Shellfish Immunology.
(45.) Creasy R. Muller C. Nantz M. . Supplementation with Aged Garlic Extract Improves Both NK and [gamma][delta]-T Cell Function and Reduces the Severity of Cold and Flu Symptoms: a Randomized, Double-Blind, Placebo-Controlled Nutrition Intervention. Clinical Nutrition.
(46.) Dalley A. Moore K. . Clinically Oriented Anatomy 5th Ed. Lippincott Williams & Wilkins: Baltimore.
(47.) Chandrashekar P. Prashanth K. Venkatesh Y. . Isolation, Structural Elucidation and Immunomodulatory Activity of Fructans from Aged Garlic Extract. Phytochemistry.
(48.) Abe A. Gu Z. Hanieh H. . Immunomodulatory Effects of Alliums and Ipomoea Batata Extracts on Lymphocytes and Macrophages Functions in White Leghorn Chickens: in Vitro Study. Animal Science Journal.
(49.) Giralt M. Llaurado M. Martin J. . Oxidative Stress in Immunocompetent Patients with Severe Community-Aquired Pneumonia. A Pilot Study. Medicina Intesnsiva.
(50.) Groff J. . Advanced Nutrition and Human Metabolism. 5th ed. Wadsworth Cengage Learning: Belmont.
(51.) Chan L. Chen Y. Chou T. . Free Radical Scavenging Activity of 4-(3, 4-dihydroxybenzoyloxymethyl.)pheny1-0-[beta]-D-Glucopyranoside from Origanum vulgare and Its Protection Against Oxidative Damage. Journal of Agriculture and Food Chemistry.
(52.) Afonso M. BEtrros S. Carvalho E. . Phenolic Compounds from Rosemary (Rosmarinus officinalis L.) Attenuate Oxidative Stress and Reduce Blood Cholesterol Concentrations in Diet-Induced Hypercholesterolemic Rats. Nutrition and Metabolism.
(53.) Ceribasi S. Ciftci M. Guvenc M. . Effects of cinnamon (Cinnamomum zeylanicum.) Bark Oil on Testicular Antioxidant Values. Apoptotic Germ Cell and Sperm Quality, Andrologia.
(54.) Chuang L. Li R. Yang C. . Antioxidant Activity of Various Parts of Cinnamomum cassia Extracted with Different Extraction Methods. Molecules.
(55.) Gonzalez de Mejia E. Johnson M. . Comparison of Chemical Composition and Antioxidant Capacity of Commercially Available Blueberry and Blackberry Wines in Illinois. Journal of Food Science.
(56.) Ghasemzadeh A. Ibrahim M. Jaafar H. . Combined Effect of CO2 Enrichment and Foliar Application of Salicylic Acid on the Production and Antioxidant Activities of Anthocyanin, Flavonoids and Isoflavonoids from Ginger. BMC Complementary and Alternative Medicine.
(57.) Bak M. Jeong W. Jun M. . 6-Shogaol-Rich Extract from Ginger Up-Regulates the Antioxidant Defense Systems in Cells and Mice. Molecules.
(58.) Chen R. Guo S. Liu J. . S-Allyl Cysteine Restores Erectile Function Through Inhibition of Reactive Oxygen Species Generation in Diabetic Rats. Andrology.
(59.) Chen T. Guan J. Liu J. . Neuroprotective Effects of Allicin on Spinal Cord Ischemia-Reperfusion Injury via Improvement of Mitochondrial Function in Rabbits. Neurochemistry International.
(60.) Aquilano K. Baldelli S. Ciriolo M. . Neuronal Nitric Oxide Synthase Protects Neuroblastoma Cells from Oxidative Stress Mediated by Garlic Derivatives. Journal of Neurochemistry.
(61.) Xie K. Zeng T. Zhao X. . Garlic Oil Attenuated Nitrosodiethylamine-Induced Hepatocarcinogenesis by Modulating the Metabolic Acti ation and Detoxification Enzyems. international Journal of Biological Sciences.
(62.) Dhawan V. Jain S. . Garlic Supplementation Prevents Oxidative DNA Damage in Essential Hypertension. Molecular Cellular Biochemistry.
(63.) Cavagnaro P. Camargo A. Galmarini C. [20071. Effect of Cooking on Garlic (Allium sativum L.) Antiplatelet Activity and Thiosulfinates Content. Journal of Agriculture and Food Chemistry.
(64.) Chohan M. Forster-Wilkins G. Opara E. . Determination of the Antioxidant Capacity of Culinary Herbs Subjected to Various Cooking and Storage Processes using ABTS(*+) Radical Cation Assay. Plant Foods and Human Nutrition.
(65.) Centers for disease control. . Foodborne Illness, Foodborne Disease, (sometimes called "Food Poisoning".). Accessed at the URL: http://www.cdc.gov/foodsafety/facts.html#howmanycases
(66.) Centers for Disease Control. . CDC 2011 Estimates: Findings.  Accessed at the URL: http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html
(67.) Department of Health. . Report on a Survey of Spices for the Presence of Pathogens, Department of Health, Victoria, Australia. Accessed at the URL: http://www.health.vic.gov.au/archive/archive2011/foodsalety/archive/downloads/survey_spices.pdf
(68.) Kisluk G. and Yaron S. . Presence and Persistence of Salmonella enterica Serotype Typhimurium in the Phyllosphere and Rhizosphere of Spray Irrigated Parsley. Application of Environmental Microbiology.
(69.) Centers tbr Disease Control. . Salmonella Montevideo Lnfections Associated with Salami Products Made with Contaminated Imported Black and Red Pepper---United States, July 2009--April 2010.
(70.) Zweifel, C. Stephan R. . Spices and herbs as source of Salmonella-related foodborne diseases. Food Research International.
(71.) Sagoo, S.K. Little C.L. Greenwood M. . Assessment of the Microbiological Safety of Dried Spices and Herbs from Production and Retail Premises in the United Kingdom. Food Microbiology.
(72.) Hara-Kudo Y. Ohtuska K. Onoue Y. . Salmonella Prevalence and Total Microbial and Spore Poluation in Spices Imported to Japan. Journal of Food Protection.
(73.) Moody R.K. Green S.A. Gaul, L.. National Outbreak of Salmonella Serotype Saintpaul infections: importance of Texas restaurant investigations in implicating jalapeno peppers. PLos ONE.
(74.) Higa J.. Outbreak of Salmonella Risen associated with Ground White Pepper. a Powerpoint presentation. Accessed at the URL: http://www.cdph.ca.gov/programs/DFDRS/Documents/OSS_Presentation_SRissen_and_%20white%20pepper_010611.pdf
(75.) Avery L.M. Booth P. Campbell C. . Prevalence and Survival of Potential Pathogens in Source-Segregated Green Waste Compost. Science of the Total Environment.
(76.) The U.S. Environmental Protection Agency. . Food Irradiation. Accessed at the URL: http://www.epa.gov/radiation/sources/food_irrad.html
(77.) Horvothova J. Suhaj M. Polovka M. . Effect of Gamma Irradiation on Trichromatic Values of Spices. Chemical Papers.
(78.) Brandstetter S. Berthold C. Isnardy B. . Impact of Gamma Irradiation on the Antioxidant Properties of Sage, Thyme and Oregano. Food Chemistry and Toxicology.
(79.) Calcucci L. Pinzino C. Zandomeneghi M. . Effects of Gamma-Irradiation on the Free Radical and Antioxidant Contents in Nine Aromatic Herbs and Spices. Journal of Agriculture and Food Chemistry.
(80.) Farkas J. . Irradiation as a Method for Decontaminating Food. International Journal of Food Microbiology.
(81.) National Center for Emerging and Zoonotic Infectious Diseases. . Irradiation of Food. Accessed at the URL: http://www.cdc.gov/nczved/divisions/dfbmd/diseases/irradiation_food/
(82.) Sterigenics. . The Sterilisation of Spices, Herbs and Vegetable Seasonings. Accessed at the URL: http:// www.sterigenics.com/services/food_safety/global_food_safety_brochure.pdf
(83.) Hansch G. Kotsoucliani D. Pioch M. . T Lymphocytes in Acute Bacterial Infection: Increased Prevalence of CD1 lb (+.) Cells in the Peripheral Blood and Recruitment to the Infected Site. Immunology.
(84.) Rescigno M. . Dendritic Cell Interactions with Bacteria. Cambridge University Press: New York.
by Brett R. Martin DC, MSAc and Jaya Prakash MD, MPH, SM (NRCM), SM (ASCP)
|Printer friendly Cite/link Email Feedback|
|Author:||Martin, Brett R.; Prakash, Jaya|
|Date:||Jun 1, 2013|
|Previous Article:||The legacy continues.|
|Next Article:||Sound off! Are we really winning the war on cancer?|