This study investigated biogenic amine formation in fresh vacuum-packaged beef stored at -2°C and 2°C for 100 days. The objectives were to determine the effects of storage temperature on amine production and bacterial growth, evaluate washing to reduce amine levels, and examine amine penetration into beef muscle. The main findings were: 1) Tyramine accumulated over time in both temperature groups, reaching levels that could cause intoxication after 20 days at 2°C and 40 days at -2°C. Putrescine and cadaverine were also detected. 2) Psychrotrophic bacterial and lactic acid bacteria counts increased over storage time. 3) Tyramine was detected up to

1. 284
Journal of Food Protection, Vol. 58, No.3, Pages 284-288
Copyrighl©, International Association of Milk, Food and Environmental Sanitarians
Biogenic Amine Formation in Fresh Vacuum-Packaged Beef
Stored at -2°C and 2°C for 100 Days
ANGELIA R. KRIZEK, J. SCOTT SMITH* and RANDALL K. PHEBUS
Department of Animal Sciences and Industry, Call Hall, Kansas State University, Manhattan, Kansas 66506-1600
(MS # 94-156, Received June 30, 1994/Accepted November 9, 1994)
ABSTRACT
When fresh, vacuum-packaged, meat products are stored
for extended periods of time, undesirable changes, due to
naturally occurring microbial flora present during packag-
ing occur. Lactobacillus spp. are known to form amines
through the decarboxylation of free amino acids. Tyramine
and histamine can cause intoxication in individuals taking
monoamine oxidase-inhibiting drugs. This study determined
1) the effect of storage temperature on bacterial growth and
biogenic amine production in vacuum-packaged beef
subprimals, 2) the effect of washing subprimals with water
to remove tyramine contamination, and 3) the penetration
of tyramine from the surface of the subprima1.
Inside rounds were vacuum packaged and stored at
-2°C or 2°e. Samples were evaluated over 100 days for
amine concentrations, total psychrotrophic· counts and
lactic acid bacteria. Tyramine, putrescine and cadaver-
ine were detected in this study. Significant levels (15
Ilg/g) of tyramine were detected at 20 days of storage at
2°C and 40 days of storage at -2°C. Putrescine and
cadaverine were detected first at 40 days of storage at
2°C and 60 days of storage at _2°e. Both treatment
groups contained about 130 Ilg/g of tyramine at 100
days of storage. Psychrotrophic plate counts and lactic
acid bacteria counts were initially 103
colony forming
units (CFU)/cm2
and ranged from 106
-107 CFUlcm2 at
100 days of storage-. Even though tyramine was evident
at a depth of 6 mm from the surface of the cut, one-third
of the amine was removed by washing the subprimal
with tap water.
Key words: Tyramine, putrescine, cadaverine, biogenic
amines, vacuum-packaged, beef
Food products with extended shelf lives are rapidly
gaining popularity because they are easier to market and
distribute. Advantages of vacuum-packaged fresh beef in-
clude less weight loss from evaporation, lower transporta-
tion costs, less surface trimming and longer product shelf
life (13). Current vacuum packaging technology enables
beef products to remain acceptable for consumption for
about 45 days (4). This broadens marketing potentials for
both the processor and consumer and allows more time for
products to be in transit.
However, undesirable changes, which can cause life
threatening conditions, can occur in vacuum-packaged beef
with extended shelf life. Because vacuum packaging cre-
ates an anaerobic environment, Lactobacillus and Strepto-
coccus spp. grow. Such proteolytic and decarboxylating
bacteria can produce amines known as biogenic or pressor
amines, which are normal constituents of many foods we
eat (19). Several species of lactobacilli and streptococci
demonstrate the ability to decarboxylate amino acids yield-
ing biogenic amines. These species include Lactobacillus
buchneri, Lactobacillus 30a, Lactobacillus plantarum, Lac-
tobacillus buchneri, Streptococcus faecium, Streptococcus
mitis, Streptococcus lactis and several others (17).
Excessive ingestion of histamine and tyramine has
detrimental effects on human physiological functions, most
notable headaches, flushing and acute hypertension (10). In
addition, individuals taking tranylcypromine sulfate and
monoamine oxidase-inhibiting (MAOI) drugs can suffer
from biogenic amine intoxication (9,15,18). These drugs
commonly are used as antidepressants. Tyramine toxicity
occurs more frequently than toxicity to any of the other
pressor amines in those taking MAOIs (23) and can result
in hypertensive attacks, strokes and even death (9). Al-
though little information is available for the normal popu-
lation, McCabe (9) has reported that only 6 mg of tyramine
can produce a reaction in individuals taking MAOI drugs,
and 10-25 mg can cause severe headaches to intracranial
hemorrhaging.
Biogenic amines are known to accumulate with time in
extended shelf life, vacuum-packaged beef products (16).
Studies have shown that vacuum-packaged beef stored for
7 weeks at 1°C contained measurable amounts of tyramine,
putrescine and cadaverine (3,4). In every case where tyra-
mine was detected, Lactobacillus spp. also were identified.
Edwards et a1. (3) also found that tyramine can accumulate
to detectable concentrations after extended storage at nor-
mal refrigeration temperatures, although sensory accept-
ability was prolonged.
Because vacuum packaging has played and will con-
tinue to play an integral role in the production and market-
ing of beef products, there is a need to learn how to reduce
JOURNAL OF FOOD PROTECTiON, VOL. 58, MARCH 1995

2. BIOGENIC AMINES IN VACUUM-PACKAGED FRESH BEEF 285
biogenic amine presence and production. Therefore, the
objectives of this study were determining the effects of
storage temperature on biogenic amine formation and cor-
relating tyramine production to lactic acid bacteria growth,
washing vacuum-packaged subprimals to reduce amine
levels, and penetration of amines into the muscle interior of
extended shelf life vacuum-packaged beef.
MATERIALS AND METHODS
Sampling
Beef inside rounds were purchased from a local supplier
in the Manhattan, KS, area. Each subprimal was assigned
randomly as a replicate and cut into approximately 2 in.-
thick roasts. Each roast was vacuum packaged (Model No.
A300/l6, Multivac, Inc., Kansas City, MO) in a laminated
pouch (Koch, Kansas City, MO) with an average vacuum of
599 ± 62 torr. Pouches were made of 3 mil nylon/polyethyl-
ene with an oxygen transmission rate of 4.0 cc/lOO in.2
(645.16 cm2
)/h at O°C and water vapor transmission rates of
0.6 cc/IOO in.2
(645.16 cm2
)/24 h at 37°C. Packaged samples
then were placed in storage at -2°C or 2°e.
Samples were taken before storage (day 0) and on days
10, 20, 40, 60, 80 and 100 of storage. For penetration
studies, additional samples were taken on days 60, 80 and
100. For washing studies, samples were obtained on day
100. Meat samples were obtained with 0.5 in. (1.3 cm) or
1.5 in. (3.8 cm) coring tools. The larger coring tool was
used for penetration, washing and bacteriological studies,
whereas the smaller tool was used for the amine study.
Samples were taken from an area that had no fat cover on
either side of the roast. For amine, bacteriological, and
washing studies, cores were trimmed to 10.0 g by horizon-
tally excising the middle section of the plug. For the
penetration study, the outermost ends of the core were
removed to a specified depth (3, 6 and 9 mm) from the
surface of the meat. The outermost section weights were
recorded, and amine concentrations determined. To deter-
mine the effects of removing amine contamination with
water, roasts were rinsed thoroughly with tap water under
a faucet for approximately 30 s (3.0 L/min @ 16°C). Cores
then were removed and analyzed for amine concentration.
Amines were extracted immediately from the meat
samples. Sampling of each roast was done in duplicate, and
care was taken to avoid areas containing fat cover and
connective tissue. Each treatment group (storage tempera-
ture: _2°C and 2°C; penetration: 3 mm, 6 mm and 9 mm;
and washing) contained four replicates.
Amine extraction
Amine extraction and analysis were conducted using a
modified method of Smith et al. (16). A 10.0 g sample was
obtained and placed in a Waring™ blender with 25.0 ml of
a 5% (wt/vol) solution of trichloroacetic acid and blended
at high speed for 15 s and then at medium speed for 45 s.
The sample then was filtered through a Whatman™ No. 40
fHter paper into a 50 ml volumetric flask. The flask was
brought to volume with high performance liquid chroma-
tography (HPLC) grade water. The dilutant was filtered
through a 0.22 11mnylon 66 syringe filter (Alltech Associ-
ates, Inc., Deerfield, IL) and placed in a glass vial. Samples
were frozen and later analyzed by HPLC.
Amine analysis
Amines were separated according to Van Boekel and
Arentsen-Stasse (20) as modified by Smith et al. (16) using
a Hewlett-Packard 1090A-Series II HPLC (Hewlett-Packard,
Palo Alto, CA) with a 250 mm x 4.6 mm Bio-Sil Cl8 HL-
90 reversed-phase analytical column (Bio-Rad Laboratories,
Richmond, CA). The 10 mm x 4.6 mm guard column was
packed with Bio-Sil C 18 (5 11m)material (Alltech) and fitted
with OA5-llm column frits. The system and data processing
were controlled by a Hewlett-Packard ChemStation (Pascal
series) using software HP79988A Rev. 5.22 and HP79997 A
Rev. 5.20. All HPLC solvents were "Optima" pesticide grade
or better (Fisher Scientific Co., Pittsburgh, PA).
Monoamines (tyramine, tryptamine, phenylethylamine and
histamine). These amines were separated using an isocratic
mobile phase of O.OlM I-heptane sulfonic acid and O.OIM
potassium phosphate (adjusted to pH 4.0 with IN H3
P04
) and
methanol (65:35 voVvol) at a flow rate of 1.0 mVmin. The
mobile phase was sparged continuously with helium. The
column temperature was maintained at 40°C. Amines were
detected at different wavelengths by an ultraviolet (UV)/
visible diode-array detector at 206 nm (phenylethylamine),
210 nm (histamine), and 220 nm (tyramine and tryptamine).
Identification of the amine-containing peaks were confirmed
by comparing UV sample spectra a against a spectral library
generated from pure amine standards.
Diamines (putrescine and cadaverine). Diamines were
analyzed by the method described by Jones and Gilligan (7).
Fifty IIIof amine extract solution and 50 IIIof Fluoraldehyde ™
reagent solution (Pierce, Rockford, IL) of o-phthalaldehyde
(OPA) were reacted for no longer than 45 s. Derivatized
diamines were eluted with methanol and water (70:30, voVvol)
at a 1.0 mVmin flow rate and detected by a HP l460A
programmable fluorescence detector using 231 nm excita-
tion and 425 nm emission wavelengths. Identification of
HPLC peaks containing amines were confirmed by com-
paring spectra against a spectral library generated from
pure diamine standards.
Standard solutions of tyramine, tryptamine,
phenylethylamine, histamine, putrescine and cadaverine were
prepared by dissolving an appropriate amount of the amine
hydrochloride salt (Aldrich Chemical Co., Milwaukee, WI)
in 20% methanol. All concentrations were expressed as the
free amine. Serial dilutions of the monoamines were be-
tween 1.0 Ilg/ml and 100.0 Ilg/ml, and those of the di-
amines were between 1.0 Ilg/ml and 50.0 Ilglml. A standard
curve for each amine was generated by plotting integrated
peak areas versus amine concentration. The coefficients of
determination for all standard curves were 0.994 or greater.
These generated standard curves were used to determine
the quantity of amine contamination in meat samples.
Analysis of amine accumulation consisted of duplicate
extractions that were evaluated twice to obtain an average
peak area.
Recovery of amines from beef samples was determined
by spiking 10.0 g of sirloin roast with an amount of the
amine to produce a sample concentration of 100 Ilglml.
Samples were analyzed as previously described. The mini-
mal detectable level of amines was determined to be three
times the background noise level.
JOURNAL OF FOOD PROTECTION, VOL. 58, MARCH 1995

3. 286 KRIZEK, SMITH AND PHEBUS
Bacteriological analysis
Psychrotrophic and lactic acid bacterial populations
were determined by excising a 1.5 in. (3.8 cm) diameter
core from each replicate. Between samples, tools used to
open the packages as well as the coring devices were
washed, dried, submerged in 95% ethanol for 5 min, and
flamed. The core and 90.0 ml of 0.1 % peptone water buffer
were placed together into a Stomacher bag (Spiral Biotech,
Bethesda, MD) and stomached for 2 min.
Serial dilutions of core samples were analyzed for total
psychrotrophic bacteria using plate count agar (Difco Labo-
ratories, Inc., Detroit, MI) and for lactic acid bacteria using
overlayed mithicillin-resistant Staphylococcus (MRS) agar
(Fisher). Psychrotrophic bacterial enumeration was obtained
after plates were incubated at 7°C for 10 days (5). For lactic
acid bacterial enumeration, plates were incubated at 35°C
for 48 h, and gram-positive, catalase-negative cocci or rods
were counted (6).
Statistical analysis
Statistical analysis of the data was· performed using
Least Squares Analysis of Variance (14). Dependent vari-
ables were bacterial numbers and tyramine concentrations;
independent variables were treatment and time.
RESULTS
The lowest detectable concentration for all amines from
meat samples was 1.0 Ilglg. Average recoveries from spiked
meat samples for observed amines were histamine (87.2%,
C.v. 3.3%), phenethylamine (43.1%, C.v. 6.7%), tryptamine
(23.95%, C.v. 8.1%), and tyramine (49.4%, C.v. 4.8%). No
corrections for recoveries were made on the amine levels
reported here.
Histamine, phenethylamine and tryptamine were not
detected in any of the samples. Figures I and 2 show the
levels of tyramine, putrescine and cadaverine detected in
vacuum-packaged meat samples during 100 days of stor-
age at -2 and 2°C. Tyramine was found to accumulate to
very high levels (140 Ilg/g) regardless of storage tempera-
ture. The highest measured level of tyramine was
181.1llg/g in a sample that had been stored at 2°C for 100
days. Both temperature treatments showed detectable in-
creases in tyramine concentrations starting at 20 days. The
rate of tyramine accumulation decreased at day 80.
Tyramine intoxication would be possible after 20 days of
storage at 2°C and 40 days of storage at _2°C in our
samples. It should be noted that samples stored for 100
days would be considered organoleptically inedible. Pu-
trescine was detected after 100 days of storage at average
Figure I. Biogenic amine formation in vacuum-packaged beef
stored for 100 days at -2°C (0 tyramine; 0 putrescine; L1
cadaverine). Figure 3. Lactic acid bacteria plate counts in vacuum-packaged
beef stored for lOO days at -2°C and 2°C (0 _2°C, 0 2°C).
1008040 60
Days
20
8
7
N
e6o
-5
:::::l
t;4
(93
92
1
o
o1008040 60
Days
20
160
Ci 140....
~120
-c: 100
o
iii 80•....
"E 60Q)
g 40
o
() 20
o
o
160
Ci 140
8
.... 7
~120 N
- E6
c: 100 0
0 -5:.;::;
80ctl
:::::l
•... LL.4
-c: 60 0
Q) (930
40c: 320
() 20
0
1
0 20 40 60
0
80 100 0 20 40 60 80
Days
100
Days
Figure 2. Biogenic amine formation in vacuum-packaged beef
stored for lOO days at 2°C (0 tyramine; 0 putrescine; L1
cadave rine).
Figure 4. Psychrotrophic bacteria plate counts in vacuum-pack-
aged beef stored for 100 days at _2°C and 2°C (0 -2°C, 0 rc).
JOURNAL OF FOOD PROTECTION, VOL. 58, MARCH 1995

4. BIOGENIC AMINES IN VACUUM-PACKAGED FRESH BEEF 287
TABLE I. Measurement of tyramine in penetration and washing
studies of vacuum-packaged subprimals stored at 2°C.
Days of Average J.1g1g
storage Treatment tyramine detected S.D.
60 total 10 g sample 81.9 12.4
60 3 mm penetration 103.1 42.5
60 6 mm penetration 73.0 33.2
60 9 mm penetration N.D.
80 total 10 g sample 119.5 37.2
80 3 mm penetration 124.7 64.8
80 6 mm penetration 69.6 36.2
80 9 mm penetration N.D.
100 total 10 g sample 141.4 26.7
100 3 mm penetration ]56.0 37.7
]00 6 mm penetration 131.0 5.9
100 9 mm penetration N.D.
]00 water wash* 103.2 23.0
S.D.: Standard deviation.
N.D.: Not detected.
* Subprimals were rinsed approximately 30 s on each side
with tap water.
concentrations of 99 Ilg/g at _2°C and 44 Ilg/g at 2°e.
Cadaverine was detected after 100 days of storage at
average concentrations of 27 Ilg/g at _2°C and 54 Ilg/g at
2°e.
Figures 3 and 4 illustrate lactic acid bacterial (LAB)
growth and total psychrotrophic bacterial growth with stor-
age. Initial LAB and total psychrotrophic populations were
lQ3 CFU/cm2
• Lactic acid bacteria and psychrotrophic bac-
terial growth at 2°C reached the stationary growth phase by
20 and 40 days of storage at log 6.4 and 7.2 CFU/cm2,
respectively. Bacterial populations at the -2°C storage tem-
perature appeared to reach a stationary growth phase by
approximately 60 days. Lactic acid bacteria growing at
_2°C steadily increased to log 7.5 CFU/cm2
at 80 days and
decreased to log 6.9 CFU/cm2
at 100 days of storage. In
addition, LAB and total psychrotrophic counts for samples
stored at -2°C exceeded counts for samples stored at 2°C
shortly during 40 days of storage. Statistical analysis indi-
cated that bacterial numbers were unaffected by storage
temperature over the course of the study (P<0.05). In
addition, tyramine levels were not significantly different
(P<0.05) between storage temperatures after 100 days of
storage. However, significant differences (P<0.05) in tyra-
mine levels at different storage temperatures were evident
at 20 and 40 days of storage.
Table 1 indicates the results of the washing and penetra-
tion studies. Samples stored for 100 days contained averages
of 141.41lg/g of tyramine before and 103.2 Ilg/g of tyramine
after a water rinse. Thus, rinsing caused an average reduction
of 38.21lg/g for these samples (P<0.07). Evidence of tyramine
presence at various depths from the subprimal surface ex-
plains the difficulty of using a water wash to remove tyramine.
Penetration of tyramine was evaluated after 60, 80 and 100
days of storage at depths of 0 to 3 mm, 3 to 6 mm and 6 to
9 mm. Tyramine was found in highest concentrations at the
o to 3 mm level ranging from 103 Ilg/g at 60 days to 1561lg/
g at 100 days of storage. At the second measured level of
penetration (3 to 6 mm), slightly less tyramine was found,
ranging from 73 Ilg/g at 60 days to 131 Ilg/g at 100 days of
storage. No tyramine was detected 6 to 9 mm from the
surface of the cut.
DISCUSSION
Information on biogenic amine formation in fresh,
vacuum-packaged beef stored for more than 50 days is
limited. Dainty et a1. (3) investigated the formation of
putrescine and cadaverine in vacuum-packaged beef in-
oculated with Hafnia alvei and Serratia liquefaciens for
51 days of storage at 1°e. Their inoculated study indi-
cated that putrescine reached 10 Ilg/g and cadaverine
accumulated to 200 Ilg/g. Our uninoculated study shows
the formation of these diamines but not at the same
magnitude. In addition, our study indicates that cadaver-
ine concentrations exceeded putrescine concentrations at
2°C throughout the experiment, but were reversed at _2°C.
The explanation for this interaction is unknown but prob-
ably relates to differences in predominating bacterial spe-
cies. Smith et a1. (16) and Dainty et a1. (3) showed that
biogenic amine production becomes evident when bacte-
rial loads approach log 6 CFU/cm2
• In our study, biogenic
amine formation also became apparent in all samples at
log 6 CFU/cm2 microbial load. Smith et a1. (16) measured
LAB on vacuum-packaged beef stored for 120 days at
1°e. Initial LAB counts in their study were less than 10
CFU/cm2 in comparison to log 3 CFU/cm2
for the present
study. However, after 20 days of storage at 1°C, Smith et
a1. (16) detected approximately log 4.5 CFUlcm2
LAB,
which was the first point of biogenic amine detection in
some samples. These results parallel those in our study.
When bacterial counts reached log 6 to log 7 CFU/cm2
in
both studies, bacterial growth tended to shift to the sta-
tionary phase, and amine production continued. Smith et
a1. (16) showed approximately 130 Ilg/g of tyramine after
90 days of storage at 1°C in comparison to 141 Ilg/g of
tyramine after 100 days of storage at 2°C in our study.
Edwards et a1. (3) showed a similar trend in production of
tyramine for preinoculated, vacuum-packaged, beef samples
held at 1°C for 7 weeks. They also found that tyramine
was not evident in samples until bacterial numbers ap-
proached log 6 CFU/cm2
• Edwards et a1. (4) and Rozbeh
et a1. (13) associated biogenic amine formation with
Lactococcus spp., Lactobacillus spp., Leuconostoc spp.,
Brochothrix thermosphacta, and Pseudomonas spp. in
refrigerated, fresh, vacuum-packaged beef.
Our results showed no histamine, phenethylamine and
tryptamine formation. These results agree with Edwards et
a1. (4) who reported that vacuum-packaged beef products
showed no more than 3 Ilg/g accumulation of histamine.
Vanderkerckhove (19) reported less than 7 Ilg/g of
phenethylamine in dry fermented meat products, which
caused intoxication in patients taking a monoamine oxi-
dase inhibiting drug. Tryptamine has been found in fruits,
vegetables and cheeses but generally at lower levels than

5. 288 KRIZEK, SMITH AND PHEBUS
histamine and tyramine (12). Even though tryptamine and
tyramine show similar pharmacological actions, tryptamine
intoxication has not been reported.
Rice, Eitenmiller and Koehler (1J) stated that 3.7 Ilglg
of tyramine caused intoxication in patients undergoing MAOI
drug treatment. Blackwell and Mabbit (1) determined that
5-10 mg of tyramine could cause a moderate food-drug
interaction in MAOI therapy patients. Sullivan (18) re-
ported that consumption of 6 mg of tyramine produced a
rise in blood pressure and that 10-25 mg intake induced
severe hypertension.
No reports exist for putrescine or cadaverine intoxica-
tion. However, these diamines may take an active role in
histamine intoxication and cancer promotion (2,22). Pu-
trescine and cadaverine do not directly cause intoxication
problems, but may exhibit indirect effects. Chu and
Bjeldanes (2) showed that putrescine and cadaverine po-
tentiate toxicity of histamine by increasing the rate of
histamine transport across the gut wall. Warthesen et al.
(22) reported that putrescine and cadaverine treated with
nitrite in a high temperature-low moisture system formed
nitrosopyrrolidine and nitrosopiperidine, two nitrosamines
associated with carcinogenicity. In general, these dia-
mines are used as spoilage indicators in meat products (8).
Results from this study indicate that fresh beef stored
for extended periods of time in vacuum packages can
accumulate potentially toxic levels of tyramine (>15 mg)
under normal refrigerated storage. Enough tyramine was
produced by 40 days of storage at -2°e and 20 days of
storage at 2°C to cause interactions in individuals taking
MAOI drugs. However, Taylor (19) reported that 80 mg of
tyramine can be consumed without elevation in blood
pressure by individuals not using MAOI drugs.
This research has addressed the penetration of amines
from the surface of the subprimal or the effects of washing
subprimals with water on amine concentration. Our results
indicate that amines penetrate no more than 9 mm from the
surface of the cut over 100 days of storage. The results
from our washing study also support the penetration results.
Because amines were found at various levels from the
surface of the subprimal, only 38.2 Ilg/g of tyramine was
removed by rinsing the sub primal with tap water.
CONCLUSIONS
This study indicates that biogenic amine production
should be considered when storing vacuum-packaged beef
beyond 40 days. At -2°C storage temperature, the onset of
biogenic amine formation is delayed by 20 days. However,
tyramine and putrescine concentrations are virtually the
same after 80 days of storage regardless of storage tem-
perature. Because biogenic amines do not penetrate more
than 9 mm from the surface of the subprimal, rinsing
vacuum-packaged beef with water is effective in decreasing
the amine contamination by about 30%. However, there
would still be enough tyramine present after 60 days of
storage (60 Ilg/g) so that an eight ounce portion would
contain a potentially toxic level (13.6 mg/227 g) for indi-
viduals using MAOI drugs.
ACKNOWLEDGMENTS
Contribution No. 94-537-J from the Kansas Agricultural Experiment
Station. This material is based upon work supported by The Cooperative
State Research Services, U.S. Department of Agriculture, under agreement
No. 89-34187-4511.
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