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ABSTRACT: Fruits and vegetables may contain components that exert antimicrobial effects. In this study, beef jerky
formulated with 15% raisins produced conditions inhibitory to pathogenic bacteria by decreasing pH to 5.4 and aw
to 0.64. Storage of vacuum-packaged raisin-beef-jerky (10-wk; 30 °C) resulted in a further decrease to pH 4.5 and aw
to 0.62. The antioxidant potential was increased by over 600%. The product received favorable sensory ratings for
appearance, texture, and flavor, comparable to the non-raisin control. Raisins in ready-to-eat meats such as jerky
produce a lower fat, higher fiber product with antimicrobial capability and increased antioxidant potential, thereby
providing a potentially safer, healthier alternative to traditional meat snacks.
Keywords: antimicrobial, bacteria, jerky, pathogens, raisins
taste and texture of raisins appear to be sensorially compatible with California Raisin Marketing Board (Fresno, Calif., U.S.A.). Extracts
many foods, including meat products such as jerky. for testing antimicrobial activity were made from 100g of raisins
Producers of ready-to-eat meat and poultry products must fol- using 5 different ratios (v/v) of foodgrade ethanol and water (100%,
low stringent food safety guidelines to avoid foodborne illnesses. 95%, 50%, 25%, and 10% ethanol). Samples were centrifuged, and
Jerky products must be carefully prepared, cooked, and stored to the ethanol from the supernatants was removed by low-tempera-
ensure that the product is free from potential meat pathogens (Har- ture (40 °C) vacuum distillation. Extracts prepared from California
rison and Harrison 1996; Harrison and others 2001). Pathogenic Thompson seedless raisins were evaluated for their antimicrobial
bacteria such as Staphylococcus aureus and Salmonella subsp. are activity against foodborne bacterial pathogens, yeasts, and molds.
able to survive the heat and drying treatments associated with The antimicrobial properties were estimated by individually seed-
beef jerky processing (Holley 1985). In 2000, a commercially pro- ing agar plates with each microorganism to be tested, and then
duced smoked beef jerky was voluntarily recalled in Connecticut adding 100 µL of serially diluted raisin extracts to wells bored into
when it was found to be contaminated with Listeria monocytogenes the agar. Screening of activity was also conducted using reciprocal
(FSIS 2000). In 1995, an Escherichia coli infection in Oregon was dilution tube assays to determine the lower limit of antimicrobial
traced back to the production of home-dried deer jerky (CDC 1997). activity (Daeschel 1992). Raisin purée was produced by mechani-
This jerky still tested positive for E. coli 1 year later. Jerky has also cally macerating raisins with water (10% w/w) in a food processor
been implicated in outbreaks of salmonellosis (MMWR 1985; until smooth.
MMWR 1995), and both Salmonella subsp. and L. monocytogenes
were found in beef jerky samples collected from production facili- Bacterial and fungal strains
ties between 1990 and 1999 (Levine and others 2001). Bacteria used in this study to challenge raisin extracts and raisin-
Sodium nitrite is a highly reactive compound used in meats as a jerky formulations were S. aureus (FFL #B-32), E. coli O157:H7 (ATCC
curing agent to stabilize the color, prevent rancidity and impart fla- #43895), L. monocytogenes Scott A (FFL #B-68), Salmonella cholerae-
1484 JOURNAL OF FOOD SCIENCE—Vol. 68, Nr. 4, 2003 © 2003 Institute of Food Technologists
Further reproduction prohibited without permission
Antimicrobial properties of raisins . . .
suis (ATCC #14028), and Clostridium perfringens (ATCC #12917). ature (25 °C). After 48 hrs, jerky samples were placed into Stomach-
Aerobic bacteria were grown on MacConkey-Sorbitol agar and Tryp- er® bags with 50 mL of water and pummeled at 260 rpm for 2 min
tic Soy agar. Anaerobic bacteria were grown on freshly prepared (Seward Stomacher® 400 Circulator, London, U.K.). The resulting
Brain Heart Infusion agar (BHI) using the anaerobic GasPak® sys- samples were then plated for bacterial growth on appropriate me-
tem, (Becton Dickinson, Cockeysville, Md., U.S.A.). Fungal strains dia.
included 2 species of yeast (Saccharomyces fermenti, Hansenula
polymorpha), and 5 species of mold (Geotrichum candidum, Cla- Sensory evaluation of raisin-jerky
dosporium subsp., Rhizopus nigricans, Aspergillus niger, Penicillium Freshly prepared jerky samples were evaluated for overall desir-
expansum). Yeasts were grown on Rose Bengal Chloramphenicol ability of appearance, texture, chewiness, and taste by 55 sensory
agar for 3 d at 30 °C. Geotrichum, Cladosporium, and Rhizopus were panelists in a single-blind study. The blinding codes were assigned
grown for 2 to 5 d at 25 °C on 18% glycerol agar. Aspergillus and Pen- according to a Williams block design (Williams 1949). Panelists were
icillium were grown on Malt Extract agar. asked to evaluate the flavor, texture, and chewiness of each jerky
sample on 5-point hedonic scales. The 5-point scale was chosen
Water activity and pH measurements because of the relatively large number of samples and attributes
The water activity and pH of jerky samples from the shelf-life being compared. The panelists were also asked to rank samples in
study were determined in duplicate throughout a 10-wk period. order of visual attractiveness. Demographics data (the panelist’s
Samples of each jerky formulation (approximately 2 g each) were age, gender, and frequency of consumption of jerky products) and
minced into pieces approximately 1 mm2 in size. The water activity comments were also gathered for trending. Statistical analysis of the
of each sample was determined in duplicate with a chilled-mirror responses was performed using the Compusense 5.0® software
dewpoint water activity meter (Aqualab model 3TE, Pullman, Wash., package (version 4.2, Compusense, Inc., Guelph, Canada).
U.S.A.). Each minced sample was then stirred into 10 mL of deion-
ized water for measurement of pH (Orion Research, Inc. pH model Shelf-life study of raisin-jerky
501, Boston, Mass., U.S.A.). Shelf-life studies were conducted by individually vacuum-pack-
aging 20 comparably sized pieces of each jerky formulation (raisin-
Preparation of jerky jerky, jerky-with-nitrites, and jerky-without-nitrites). Samples were
Puréed raisins were combined with lean ground beef (10% fat) to stored at 30 °C and monitored on a weekly basis for changes in
produce final raisin concentrations of 10, 15, 20, 25, and 50% (w/w). overall appearance, since the texture of jerky can undergo changes
Pepperoni-spice mix (PepperStix, Eldon Products, Kooskia, Id., related to storage temperature (Farouk and Swan 1999). Two sam-
U.S.A.) and sodium chloride were added, according to the manu- ples of each jerky formulation were removed each week for testing
facturer’s directions, to each variety of jerky to standardize the fla- (pH, aw, aerobic and anaerobic microbial growth) to document any
voring and salt concentration. Two raisin-free jerky controls were changes that might occur during storage. Total aerobic counts were
prepared, one control with sodium nitrite (0.016%) and one without. confirmed as zero by placing samples directly into Tryptic Soy Broth
Ingredients from each jerky formulation were mixed well, and (TSB) for 48 hrs, and then plating onto BHI agar to confirm sterility.
transferred to a Jerky Master (Hi Mountain Jerky, Inc., Riverton, Bacterial challenge studies were carried out to evaluate raisin-
Wyo., U.S.A.) for extrusion. Jerky strips were heated in a convection jerky’s ability to inhibit aerobic bacteria during vacuum-packaged
oven to a temperature of 200 °F for 90 min, and then allowed to cool storage. Three pathogens (S. aureus, E. coli O157:H7, and L. mono-
for 30 min before being cut into pieces (approximately 2 g each) and cytogenes) were mixed together in equal quantities, and were intro-
bagged. duced onto the surface of each 2-g jerky sample at a concentration
of approximatley 104 CFU/g. Samples were pummeled in a Stoma-
Antioxidant activity cherâ and then plated onto Tryptic Soy Agar (TSA) and MacConkey-
The antioxidant potential of a food can be measured by the Ferric Sorbitol agar, or else aseptically transferred to TSB to confirm steril-
Reducing Antioxidant Potential (FRAP) assay. In this redox reaction, ity. Enumeration of viable bacteria, together with visual
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Antimicrobial properties of raisins . . .
Surface application of raisin extracts onto beef jerky products that have an acidic pH can create a stressful environment
Commercial beef jerky was used as a food system to evaluate the for microorganisms. Low water activity in foods can also produce a
antimicrobial activity of raisin extracts when applied directly to the strong inhibitory effect. When increasing quantities of raisin purée
jerky surface. Raisin extracts were considered to be the most versa- were incorporated into ground beef, the water activity of the mix-
tile form to use with foods to evaluate potential antimicrobial activ- ture decreased (Figure 1b). However, this reduction in water activ-
ity. It was believed that a concentrated surface application of the ity was only linear (R2 = 0.92) for the uncooked raisin-jerky formu-
raisin extract would protect the exposed layer of the jerky more ef- lations. When raw beef is cooked, the water content decreases as the
fectively than integrating the extract into the meat where its anti- myofibrillar proteins shrink and undergo denaturation. This reduc-
microbial and antioxidant effects would be diluted. In theory, ap- es the water holding capacity, which reaches a minimum at the iso-
plying the raisin extracts as a dip or as a spray directly onto the jerky electric point of the muscle proteins (approximately pH 5.1) where
surface would provide the greatest protection against postprocess- there is no charge available to interact with the water (Zayas 1997).
ing surface contamination, which is a major mode of entry for micro- A nonlinear, U-shaped curve will occur when the water holding ca-
organisms found in meat products. In practice, however, the raisin pacity is plotted against cooked beef samples that have different
extracts turned out to be viscous and hygroscopic, making them pHs (Labuza 1985). When the water activity of the cooked raisin-
impossible to apply onto the surface of the jerky as an even coating. jerky samples was graphed against the pH (Figure 2), a typical U-
Jerky strips treated with raisin extract became sticky and attracted shaped curve was produced with endpoints representing 100%
moisture to the surface, thereby increasing the water activity and ground beef (pH 5.8; aw 0.91) and 100% raisin purée (pH 4.0; aw
promoting, rather than inhibiting, microbial growth. Consequently, 0.58). The lowest point on the curve (pH 4.7; aw 0.42) suggests that
it became necessary to incorporate the raisins directly into ground raisins can decrease the isoelectric point of ground beef, thereby
beef to produce a raisin-jerky product. decreasing the water activity of the cooked jerky. Formulations con-
taining approximately 35% raisin purée would be needed to
Incorporation of raisin purée into ground beef achieve the minimum water activity.
The pH of the raisin-jerky formulations decreased linearly with
increasing concentrations of raisin purée in both uncooked and Microbial evaluation of raisin-jerky
cooked samples (Figure 1a). Raisins contain substantial amounts of The antimicrobial properties of 2 raisin-jerky concentrations were
organic acids, which contribute to their low pH (3.5 to 4.0). Food tested by challenging with S. aureus. Antibacterial activity was
found to be directly related to the decrease in water activity that
occurred in the presence of the raisin purée (Figure 3). S. aureus is
found on a high percentage of raw meat, however it neither grows
nor produces enterotoxin when the surrounding water activity is
less than 0.83 (Bergdol 1989). This suggests that beef products such
as jerky would not be conducive to growth for S. aureus when at
least 10% raisins are present.
A similar decrease in bacterial survival was observed when E. coli
O157:H7 and L. monocytogenes were used to challenge raisin-jerky
formulations (Figure 4). Despite the low pH and water-activity val-
ues measured earlier, the inoculated jerky samples appeared to
allow substantial bacterial growth. When the initial bacterial sus-
pension was applied onto the surface of the jerky, it raised the water
activity and allowed a higher rate of bacterial survival. The approx-
imate increase in water activity was determined by inoculating
each variety of jerky with sterile water (0.1 ml/g), and allowing the
Food Microbiology and Safety
1486 JOURNAL OF FOOD SCIENCE—Vol. 68, Nr. 4, 2003 JFS is available in searchable form at www.ift.org
Antimicrobial properties of raisins . . .
levels, beef jerky containing raisin purée still compromised bacte- Table 1—Summary of sensory evaluation by 55 panelists
rial survival as shown in Figure 4. of beef jerky samples formulated with nitrite or raisins at
different concentrations
Sensory panel results for raisin jerky Sensory Nitrite 10% 15% 20%
Panelists ranked the 10% raisin jerky as superior to the nitrite- Attribute control Raisins Raisins Raisins
cured control in terms of overall liking, flavor, texture, and appear- Flavor 1 3.4 (1.3)ab 3.6 (1.1) a 3.2 (1.0)ab 3.0 (1.1) b
ance ( Table 1). Written comments indicated that the sweet and Texture 1 3.6 (1.0) a 3.8 (0.9) a 3.6 (1.0) a 2.8 (1.2) b
Chewiness 1 2.9 (0.8) a 3.0 (0.6) a 2.7 (0.8)ab 2.4 (1.0) b
tangy flavor imparted by the raisins was pleasing, and reduced the
Overall Liking1 3.4 (1.2) a 3.7 (1.0) a 3.3 (0.9)ab 2.8 (1.2) b
perceived saltiness of the jerky. The 20% raisin jerky was consistent- Appearance2 3rd 1st (best) 2nd 4th (worst)
ly scored lower than the other samples in all sensory categories, and 1 Mean score on a hedonic scale from 1 (dislike greatly) to 5 (like greatly)
was described as crumbly or too soft in texture, with an “unusual” 2 Panelists were asked to rank a set of 4 samples in order from most to least
visually appealing.
or overly sweet flavor. The jerky formulated with 15% raisins was Standard deviation is given in parentheses. Samples with like letters do not
judged positively for all characteristics except chewiness, and thus differ significantly. For all samples, n = 55 and p < 0.03.
appears to be the limit of consumer acceptability. Approximately
60% of the respondents claimed to eat jerky products at least once
every 3 mo.
Shelf-life studies This was likely initiated during the heating and cooling processes
Shelf-life studies were conducted to monitor changes in appear- before the jerky was packaged. As moisture evaporated from the
ance, texture, pH, water activity, and antimicrobial activity of vac- hot jerky, water was drawn from the inner regions of the meat,
uum-packaged raisin-jerky (15%) and 2 controls. One control was bringing salts with it to the surface (Ledward 1981). Concentrations
prepared using a curing mix containing 6.22% sodium nitrite, and of salt on the surface would directly affect the ionic strength, and
the other control was formulated without nitrites. cause a change in the pH of the jerky, which may have contributed
Initially, cooked samples of both nitrite-treated and nitrite-free to the decreased pH observed during 10-wk of storage.
controls had pH values above 6.0, while the 15% raisin-jerky had a As part of the shelf-life study, uninoculated jerky samples were
pH of 5.4 (Figure 5). Over the course of the 10-wk study, the pH tested for microbial growth. None of the samples initially harbored
dropped to 5.5 for the controls and to pH 4.5 for the raisin-jerky. any viable aerobic or anaerobic bacteria, nor were any bacteria re-
Both pH and aw of vacuum-packaged meats are known to decrease covered during the 10-wk study. To evaluate the microbial safety of
with storage time (Papadopoulos and others 1991; Blixt and Borch raisin-jerky in the event of post-processing contamination, 15%
2002). In this study, the water activities of each jerky variety also raisin-jerky and 2 controls were challenged with 3 pathogenic bac-
decreased over time (Table 2). The high residual sugar concentra- teria (E. coli O157:H7, L. monocytogenes, and S. aureus) before vac-
tion in raisins contributes to increased osmotic pressure and de- uum packaging. The initial water activity for each jerky formulation
creased water activity in any product that incorporates them. Low was below 0.75 (Table 2). The low water activity and anaerobic en-
aw beef jerky will be microbiologically safer, however these meats vironment within the vacuum packaging resulted in no aerobic
tend to be unacceptably tough and chewy. The addition of raisins bacteria being recovered after 4 wk (Figure 6). Although it has been
produced a low water activity while retaining a softer, more pliable found that E. coli O157:H7 contaminants are less able to survive
texture. when jerky is formulated with a nitrite and salt cure mix (Harrison
Within a few weeks of storage, the formation of salt crystals was and others 1998), the raisin-jerky was equally effective at inhibiting
observed on the surfaces of all 3 vacuum-packaged jerky varieties. E. coli O157:H7 (as well as 2 other meat-borne pathogens L. mono-
cytogenes and S. aureus). It has also been observed that E. coli
O157:H7 contaminants are less able to survive in jerky formulated
with a low fat content (Faith and others 1998). This suggests that
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Antimicrobial properties of raisins . . .
Table 2—initial and final water activity of jerky samples over sodium nitrite is allowed only in certain foods, at a concentration of
10-wk study 156 g NaNO2 per g of food (CFR 2001).
Jerky samples Initial aw Final aw
Nitrite control 0.73 ± 0.01 0.61 ± 0.01
Antioxidant activity of raisin-jerky
Nitrite-free control 0.74 ± 0.01 0.66 ± 0.01 Harmful reactive oxygen species and free radicals, which are by-
15% Raisins 0.64 ± 0.01 0.62 ± 0.01 products of normal aerobic metabolism, are commonly associated
with human cell damage and aging. Antioxidant compounds in
foods can help prevent oxidative damage (Mathews and others
2000). Grapes and raisins are known to contain high levels of anti-
oxidants because of their polyphenol content. (Wang and others
15%-raisin jerky (with 15% less fat than the raisin-free control 1996). In this study, jerky samples formulated with 15% raisins had
jerkys) would prove especially effective at controlling the growth of antioxidant values over 600% higher than the control samples for-
E. coli O157:H7. mulated without raisins (Figure 7). The high antioxidant levels in
Clostridium perfringens spores present in foods may survive the
heating process and eventually germinate in the gastrointestinal
tract and produce enterotoxins (McClane and Rood 2001). To ver-
ify that bacterial spores cannot survive and produce toxins in vac-
uum-packed raisin-jerky, challenge studies were conducted using
an anaerobic sporeformer (C. perfringens). This microorganism was
chosen because its spores can be unintentionally introduced into
food products through the addition of flavorings and spices. The
initial pH of raisin-jerky was 5.4 and the final pH was 4.5 (Figure 5).
Below pH 5.5, C. perfringens growth is inhibited, and below pH 5.0,
cells die within a few days (Wrigley 1994). This suggests that the
addition of raisins to meat products may protect against the growth
of anaerobic sporeformers.
The jerky treated with nitrites had less than 40 CFU/g C. perfrin-
gens at week 5, whereas the control jerky formulated without ni-
trites or raisins still had C. perfringens counts at 103 CFU/g. By the
6th wk, all of the vacuum-packed jerky samples had bacterial counts
less than 40 CFU/g. Gram stains and phase-contrast microscopy
were initially used to determine if spores were forming in viable C.
perfringens cells, however since C. perfringens generally does not
sporulate in foods, no spores were ever detected in the raisin-jerky.
Additionally, since C. perfringens enterotoxin is only produced dur-
ing sporulation (which typically occurs in the intestine after con-
sumption of viable cells) and is generally not present in the con-
taminated food, this study concentrated on the recovery of viable
C. perfringens. Based on this survival study, we anticipate that other
Clostridium subsp., (for example, C. botulinum), would be similarly
inhibited by a raisin-jerky product that is free of nitrites. In the U.S.,
Food Microbiology and Safety
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Antimicrobial properties of raisins . . .
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