Food Microbiology 50 (2015) 1e4

Contents lists available at ScienceDirect

Food Microbiology
journal homepage: www.elsevier.com/locate/fm

Inactivation of avirulent Yersinia pestis on food and food contact

surfaces by ultraviolet light and freezing*
Christopher H. Sommers*, Shiowshuh Sheen
U.S. Department of Agriculture, Agricultural Research Service, Eastern Regional Research Center, 600 East Mermaid Lane, Wyndmoor, PA 19038, USA

a r t i c l e i n f o a b s t r a c t

Article history: Yersinia pestis, the causative agent of plague, can occasionally be contracted as a naso-pharyngeal or
Received 31 July 2014 gastrointestinal illness through consumption of contaminated meat. In this study, the use of 254 nm
Received in revised form ultraviolet light (UV-C) to inactivate a multi-isolate cocktail of avirulent Y. pestis on food and food contact
16 January 2015
surfaces was investigated. When a commercial UV-C conveyor was used (5 mW/cm2/s) 0.5 J/cm2 inac-
Accepted 14 February 2015
tivated >7 log of the Y. pestis cocktail on agar plates. At 0.5 J/cm2, UV-C inactivated ca. 4 log of Y. pestis in
Available online 21 February 2015
beef, chicken, and catfish, exudates inoculated onto high density polypropylene or polyethylene, and
stainless steel coupons, and >6 log was eliminated at 1 J/cm2. Approximately 1 log was inactivated on
Keywords:
Yersinia pestis
chicken breast, beef steak, and catfish fillet surfaces at a UV-C dose of 1 J/cm2. UV-C treatment prior to
Ultraviolet freezing of the foods did not increase the inactivation of Y. pestis over freezing alone. These results
Food indicate that routine use of UV-C during food processing would provide workers and consumers some
Food contact surfaces protection against Y. pestis.
Beef Published by Elsevier Ltd.
Chicken
Catfish

1. Introduction processing intervention technologies to inactivate Y. pestis in food

Yersinia species including Yersinia enterocolitica, Yersinia pseu-
dotuberculosis, and Yersinia pestis are closely related species which
can cause illness in humans (Paoli and Sommers, 2014). Of those 3,
Y. pestis is the causative agent of plague and can cause pharyngeal
or gastrointestinal infection through the handling or consumption
of meat products (Leslie et al., 2010; Albaji et al., 2005; Bin Saeed
et al., 2005; Christie et al., 1980). The risk, and the associated
morbidity and mortality, of contracting plague through the con-
sumption or handling of foods deliberately contaminated with
Y. pestis are currently unknown. Because Y. pestis is listed as a select
agent for both food safety and food defense (Brickner et al., 2003;
Khan et al., 2000; Kauffman et al., 1997; WHO, 1970) it would
therefore be prudent to evaluate the efficacy of nonthermal food
*
Mention of trade names or commercial products in this publication is solely for
the purpose of providing specific information and does not imply recommendation
or endorsement by the U.S. Department of Agriculture. USDA is an equal oppor-
tunity provider and employer.
* Corresponding author. Food Safety and Intervention Technologies Research
Unit, Eastern Regional Research Center, USDA-ARS, 600 East Mermaid Lane,
Wydnmoor, PA 19038, USA.
E-mail address: christopher.sommers@ars.usda.gov (C.H. Sommers).
products.
Recent studies have investigated the ability of Y. pestis to grow in
foods, including growth at refrigeration temperature. Bhaduri and
Phillips (2013) found that Y. pestis KIM5 did not grow in refriger-
ated ground pork (4
C), but was able to grow at the mild refrig-
eration abuse temperatures of 10 and 15
C at ca. 0.05 and 0.16 log10
CFU/h, respectively. Y. pestis KIM5 readily grew at 20, 25 and 30
C
at 0.26, 0.30 and 0.77 log10 CFU/h. Sommers and Cooke (2009)
found that Y. pestis was capable of growth on frankfurters at
10
C, while Gurtler et al. (2010) found Y. pestis capable of growth in
refrigerated liquid egg. Torosian et al. (2009) found that Y. pestis
was capable of growth in Brain Heart Infusion Broth at 4
C.
Other studies investigated the use of both thermal and non-
thermal intervention technologies to inactivate Y. pestis in foods.
Sommers and Niemira (2007) investigated the use of gamma ra-
diation at both refrigeration (D10 0.19 at 10
C) and frozen tem-
peratures (D10 0.37 kGy at 20
C) and developed a predictive
equation to describe the temperature dependent radiation inacti-
vation kinetics of Y. pestis in ground meat. Sommers and Cooke
(2009) found the gamma radiation D10 of a multi-isolate cocktail
of Y. pestis inoculated onto phosphate buffer and frankfurters to be
0.23 and 0.31 kGy, respectively. Porto-Fett et al. (2009) determined
the thermal D10 value of Y. pestis KIM5 suspended in 75% lean

http://dx.doi.org/10.1016/j.fm.2015.02.008
0740-0020/Published by Elsevier Ltd.
2 C.H. Sommers, S. Sheen / Food Microbiology 50 (2015) 1e4
ground beef at 48.9e60
C to range from 193 to 0.56 min, respec-
tively, with a z-value of 4.57
C.
Ultraviolet light (UV-C, 254 nm), a U.S. Food and Drug Admin-
istration (FDA) approved food safety intervention technology, can
be used for decontamination of food and food contact surfaces (CFR,
2005). UV-C exerts its bacteriocidal effect primarily through the
formation of DNA adducts including cyclobutane pyrimidine di-
mers and 6e4 photoproducts, either killing the bacteria or
rendering them unable to reproduce, and to some extent through
oxidation of proteins in the bacterial cell (Reardon and Sancar,
2005; Krisko and Radman, 2010). The technology has been
increasingly adopted by the health care industry for decontami-
nation of surfaces in medical facilities and in recent years the food
processing industry has expressed significant interest in using it for
surface decontamination of foods and food contact surfaces in the
food processing environment (Salvage, 2014; Rutala et al., 2010;
Koutchma, 2008; Koutchma et al., 2008). UV-C is of particular ap-
peal to the medical and food processing industries because it is a
green and sustainable technology which does not require the use of
water or chemicals to exert its bacterial effects.
While a great deal of information is available on the use of ul-
traviolet light (UV-C) to inactivate common foodborne pathogens
(Sommers et al., 2010; Sumner et al., 1996; Stermer et al., 1987),
relatively little information is available on the inactivation of
Y. pestis on foods with ultraviolet light. The purpose of this study
was to determine the ability of Y. pestis to survive treatment with
UV-C on agar plates, food contact surfaces, and foods using a
commercial UV-C conveyor.
2. Materials and methods
2.1. Food products
Catfish fillets (2e3 oz) were obtained from the USDA-ARS Cat-
fish Genetics Laboratory in Stoneville, Mississippi. Beef steaks (3e4
oz) and boneless skinless chicken breast fillets (3e4 oz) were ob-
tained fresh from a local butcher. The meat, poultry, and ready-to-
eat meat products were gamma irradiated to an absorbed dose of
5 kGy at 4
C to inactivate background microflora, which was
reduced to less than to <0.1 CFU/g as determined by plating on
Brain Heart Infusion agar (BD-Difco, Sparks, MD). Exudate (drip/
purge) was obtained from the irradiated products by pouring
excess liquid into sterile test tubes. Food was stored at 0e4
C until
ready for use, while exudates were stored at 20
C.
2.2. Avirulent Yersinia pestis isolates
Four avirulent Y. pestis strains (KUMA, Yokohama, KIM5, and
CO99) were obtained from Dr. Susan Straley (Univ. Kentucky) and
Dr. Robert Brubaker (Mich. State Univ.) through Dr. George Paoli at
USDA's Eastern Regional Research Center (Wyndmoor, PA). The
Y. pestis strains were propagated on Brain Heart Infusion Agar
(BHIA) (BD-Difco, Sparks, MD) at 30
C for approximately 3 days
and maintained at 0e4
C until ready for use.
2.3. Propagation and inoculation
Each Y. pestis strain was cultured independently in 30 ml BHI
Broth (Brain Heart Infusion, BD-Difco, Sparks, MD) in a sterile 50-
mL conical tube at 30
C (150 rpm) for 36 h, to a density of
approximately 108 CFU/ml, using a New Brunswick Model G24
Incubator (Edison, NJ). The cultures were then sedimented by
centrifugation (1200  g) using a Fisher Scientific Marathon
21000R Centrifuge (Needham Heights, MA). The cell pellets were
then resuspended as a cocktail in 30 mL Butterfield's Phosphate
Buffer (BPB) (Applied Research Institute, Newtown, CT).
One hundred mL (0.1 mL) of the Y. pestis undiluted cocktail was
plated onto duplicate BHIA plates which were then allowed to dry
for approximately 5 min. The agar plates were then exposed to 0.5 J/
cm2 UV-C using the UV-C conveyor as described below.
For experiments using exudates on high density polypropylene
(HDPP) and polyethylene (HDPE) and stainless steel coupons (bead
blasted and electropolished) 0.1 mL of Y. pestis cocktail was pipetted
into 0.9 mL of the sterile food exudates, mixed by vortexing for ca.
10 s, and 0.1 mL transferred to the chilled (4
C) food contact sur-
faces and exposed to UV-C as described below. Prior to experi-
mentation stainless steel coupons were sterilized by autoclaving
while HDPP and HDPE were cleaned with 70% ethanol and then
subjected to 10 J/cm2 UV-C.
Chicken, fish, and beef pieces were inoculated on one side of the
surface with 1.0 mL (ca. 106 CFU/ml), which was then spread on the
food surface (3  3 cm) using a sterile inoculation loop. The inoc-
ulated pieces were allowed to sit in a refrigerator (4
C) for ca. 30
min, and then passed through the conveyor to obtain the required
UV-C doses (0.25, 0.5, 1.0 and 2.0 J/cm2).
Following exposure to UV-C, food samples were placed in sterile
polynylon bags (Uline, Inc., Philadelphia, PA) containing 100 ml BPB
and rinsed manually by massaging for ca. 30 s. The solution was
then serially diluted in 9 ml BPB and two 0.1 mL aliquots per
dilution were spread on BHI agar plates (BD-Difco, Sparks, MD). The
plates were then incubated for 3 days at 30
C prior to enumeration
of bacterial colonies. Each experiment was conducted indepen-
dently a minimum of 3 times (n ¼ 3).
2.4. Exposure to ultraviolet light (UV-C)
A commercial food-grade UV-C conveyor (Reyco Systems, Inc.,
Meridan, ID) was used to treat exudates inoculated with avirulent
Y. pestis on surfaces of BHI agar plates, stainless steel coupons, HDPP
and HDPE, and the foods themselves. The UV-C intensity was
5 mW/s/cm2, and 100 s of exposure provided a total UV-C dose of
approximately 0.5 J/cm2. All experiments were conducted in a BSL-
2 laboratory.
The exudates (0.1 mL, ca. 107 CFU) were inoculated onto BHI agar
plates, stainless steel or polypropylene coupon surfaces were run
through the conveyor either once, twice or four times to obtain ex-
posures of 0.5 J/cm2, 1.0 J/cm2 or 2.0 J/cm2, respectively. Beef steaks,
chicken breast, and catfish fillets were passed through the conveyor
up to 4 times to obtain the maximum UV-C dose of 2.0 J/cm2.
UV-C intensity was monitored using a calibrated UVX Radiom-
eter (UVP Inc., Upland, CA). The temperature of the room was
approximately 15
C during the exposure to UV-C, and the food
temperature did not increase to more than 15
C at the end of the
process as measured using an infrared thermometer.
2.5. Freezing
Catfish fillets, chicken breasts, and beef steaks were inoculated
and treated with UV-C as described above and then frozen using
dry ice. The individual samples were then packaged in polynylon
bags (Uline Inc., Philadelphia, PA), sealed using a Multi-Vac 300
packager to ca. 5000 Pa and stored at 20
C for ca. 30 days. To
assess bacterial counts after freezing, the samples were thawed in a
refrigerator (ca. 4
C) overnight.
2.6. Statistical analysis
Log reductions were determined according to Diehl (1995). Each
experiment was conducted independently a minimum of 3 times.
 C.H. Sommers, S. Sheen / Food Microbiology 50 (2015) 1e4
Statistical analysis functions of MS Excel (Microsoft Corp., Red-
mond, WA) were used for routine calculations, descriptive statis-
tics, and ANOVA.
3. Results and discussion
In this study the use of UV-C light to inactivate a multi-isolate
cocktail of Y. pestis on agar plates, food contact surfaces, and
foods using a commercial UV-C conveyor was investigated. Rose
and O'Connell (2009) found that a UV-C dose of 4 mJ/cm2 inacti-
vated 4.9 and 4.4 log of Y. pestis A112 and Harbin suspended in
sterile distilled water, respectively, indicating a D10 of ca.
0.5e1.0 mJ/cm2 Paoli and Sommers (2014) obtained D10 of
0.69e1.02 mJ/cm2 for Y. pestis KIM5 or Yokohama, which either
contained or lacked the high pathogenicity island encoding several
proteins necessary or iron acquisition (PGMþ and Dpgm), on Congo
Red Agar Plates. In both of those studies low intensity lab-scale
(<100 uW/cm2) UV-C sources were used to determine D10. When
Y. pestis was inoculated onto agar plates and treated with 0.5 J/cm2
UV-C at an intensity of 5 mW/cm2/s using a UV-C conveyor >7 log
were inactivated.
The next set of experiments investigated the ability of UV-C to
inactivate Y. pestis suspended in exudates (drip) from chicken
breast, beef steak, and catfish fillets. Because the exudates was
relatively transparent, UV-C was able to fully penetrate (>95%) all of
the exudates to a depth of 2 mm. When the exudates were placed
on bead blasted, electropolished, HDPE, and HDPP coupons, ca. 4
log inactivation of Y. pestis was obtained, with no significant dif-
ference (p > 0.05) in inactivation for the type of food contact surface
used or exudate used (Table 1). A >6 log reduction was obtained on
bead blasted, electropolished stainless steel, HDPE, and HDPP at a
dose of 1.0 J/cm2, which was essentially a complete inactivation
(data not shown). The lower inactivation levels compared to agar
plates could be due to shadowing from particulate matter within
the exudates.
Inactivation of microorganisms on actual foods is much more
difficult due to food surface topology and shadowing, which shields
them from UV-C light (Gardner and Shama, 2000). In previous work
in our laboratory we obtained ca. 0.5 log reduction of Salmonella,
Staphylococcus aureus, Listeria monocytogenes, or Francisella tular-
ensis on previously frozen chicken meat, beef steak, or catfish fillets
(Sommers et al., 2012, 2010). In this study, refrigerated (never
frozen) catfish, poultry, and beef were used to avoid potential
surface topology changes due to freezing and freezer burn. In this
study ca. 0.75e1 log reductions were obtained at 1 J/cm2 UV-C
(Fig. 1). While slightly greater inactivation was obtained at 2 J/
cm2, there was no statistical significance as determined by ANOVA
(p > 0.05). As in our previous studies, there is no advantage to
applying UV-C doses in excess of 1 J/cm2 to the meat, poultry and
fish products.
However, contamination of foods with microorganisms is also
due to transfer from food contact surfaces to the actual foods during
Table 1
UV-C (0.5 J/cm2) inactivation of avirulent Y. pestis suspended in exudates on stainless
steel and plastic.
Catfish Beef Chicken
Bead Blasted-SS 4.04 (±0.06) 3.91 (±0.11) 3.87 (±0.23)
Electropolished-SS 3.94 (±0.14) 4.03 (±0.29) 3.71 (±0.12)
HDPE 3.99 (±0.21) 3.78 (±0.16) 3.83 (±0.09)
HDPP 4.01 (±0.26) 3.76 (±0.13) 3.75 (±0.19)
Each experiment was conducted independently 3 times. Values are log10 reductions
as compared to the untreated controls with the standard error of the mean in
parenthesis. There was no statistical difference in the log10 reductions as deter-
mined by ANOVA (p > 0.05).
3
Fig. 1. Inactivation of avirulent Yersinia pestis on foods by ultraviolet light (UV-C). UV-C
doses for beef (B), chicken (C), catfish (D)were 0.25, 0.5, 1.0 and 2.0 J/cm2. Each
experiment was conducted independently 3 times. Standard deviation is shown as
error bars.
processes. The use of UV-C allows a waterless and chemical-free
method of decontaminating food contact surfaces such as HDPE,
HDPP, and stainless steel, or more specifically the purge from the
food products which lie on the food contact surfaces. Our results
demonstrate the potential of UV-C for decontamination of purge
and food contact surfaces. To date there has been little published
data on the use of UV-C to inactivate microorganisms suspended in
purge which contaminates food contact surfaces. Sommers and
Gunther demonstrated a >5 log reduction of Campylobacter jejuni
suspended in poultry exudate on food contact surfaces by UV-C
(Sommers and Gunther, 2013) These results are similar to UV-C
inactivation obtained in similar experiments using the biothreat
agent F. tularensis (Sommers et al., 2012), in which a >5 log
reduction of F. tularensis was obtained in purge from meat, poultry,
and catfish. It may be useful to examine the use of UV-C in com-
bination with natural antimicrobials for inactivation of microor-
ganisms within food product exudate in the future.
Because beef, chicken and fish can be frozen either before or
after packaging, we wanted to determine the effect of UV-C appli-
cation prior to freezing. Previous studies with other foodborne
pathogens have indicated a ca. 1e2 log reduction as a result of
freezing (Rajkowski and Sommers, 2012; Sommers et al., 2011). In
this study a ca. 1 log reduction of Y. pestis was obtained regardless of
food matrix type (p > 0.05) (Table 2). As is shown in Fig. 1, a ca. 1 log
reduction of Y. pestis was obtained regardless of food matrix type
after 1 J/cm2 UV-C. There was no additional log reduction as a result
of UV-C exposure followed by freezing (p > 0.05) (Table 2), how-
ever, we did note that recovery of the Y. pestis required an addi-
tional day of incubation on the Brain Heart Infusion Agar.
Table 2
Effect of freezing on survival of avirulent Y. pestis with and without UV-C treatment.
Catfish Beef Chicken
UV-C (1 J/cm2) 1.10 (±0.03) 1.12 (±0.06) 1.07 (±0.09)
Freezing 1.03 (±0.02) 0.96 (±0.04) 1.07 (±0.08)
UV-C þ Freezing 1.21 (±0.10) 1.20 (±0.05) 1.04 (±0.09)
Each experiment was conducted independently 5 times. Values are log10 reductions
as compared to the untreated controls with the standard error of the mean in
parenthesis. There is no statistical difference in the log10 reductions as determined
by ANOVA (p > 0.05).
4 C.H. Sommers, S. Sheen / Food Microbiology 50 (2015) 1e4
4. Conclusions
Using a UV-C conveyor system we were able to demonstrate a
4e6 log reduction of avirulent Y. pestis suspended in beef, chicken,
and poultry drip (purge) on stainless steel and plastic surfaces at a
dose of 0.5e1.0 J/cm2. A ca. 1 log reduction of avirulent Y. pestis was
obtained on boneless skinless chicken breasts, beef steaks, and
catfish fillets. These results are consistent with other studies indi-
cating that use of UV-C can significantly decontaminate exudates
on food contact surfaces, and foods, during processing.
Acknowledgments
We would like to thank Robert Richardson for his technical
assistance.
References
Albaji, A., Kharabsheh, S., Al-Azab, S., Al-Kayad, M., Amr, Z., Abu-Baker, M., Chu, M.,
2005. A 12-case outbreak of pharyngeal plague following consumption of camel
meat, in north-eastern Jordan. Ann. Trop. Med. Parasitol. 99 (8), 789e793.
Bhaduri, S., Phillips, J., 2013. Growth of pYV bearing Yersinia pestis KIM5 in retail
ground pork. Foodborne Pathog. Dis. 10 (5), 467e471.
Bin Saeed, A., Al-Hamdan, N., Fontaine, R., 2005. Plague from eating raw camel liver.
Emerg. Infect. Dis. 11 (9), 1456e1457.
Brickner, P., Vincent, R., First, M., Nardell, E., Murray, M., Kaufman, W., 2003. The
application of ultraviolet germicidal irradiation to control transmission of
airborne disease: bioterrorism countermeasure. Public Health Rep. 118, 99e114.
Christie, A., Chen, H., Elberg, S., 1980. Plague in camels and goats; their role in
human epidemics. J. Infect. Dis. 141, 724e726.
CFR (Code of Federal Regulations), 2005. Irradiation in the production, processing
and handling of food. Code Fed. Regul. 21 (179), 450e456.
Diehl, J., 1995. Safety of Irradiated Food, second ed. Marcel Dekker, New York, New
York, pp. 93e98.
Gardner, D., Shama, G., 2000. Modeling UV-induced inactivation of microorganisms
on surfaces. J. Food Prot. 63, 63e70.
Gurtler, J., Rivera, R., Zhang, H., Sommers, C., 2010. Behavior of avirulent Yersinia
pestis in liquid whole egg as affected by storage temperature, antimicrobials
and thermal pasteurization. J. Food Saf. 30, 537e557.
Kauffman, A., Meltzer, M., Schmid, G., 1997. The economic impact of a bioterrorist
attack:are prevention and post attack programs justifiable. Emerg. Infect. Dis. 3,
83e94.
Khan, A., Morse, S., Lillibridge, S., 2000. Public-health preparedness for biological
terrorism in the USA. Lancet 356, 1179e1182.
Koutchma, T., Forney, L., Moraru, C., 2008. Microbial inactivation by UV light. In:
Ultraviolet Light in Food Technology. Taylor & Francis CRC Press, New York, New
York, USA, pp. 69e99.
Koutchma, T., 2008. UV-C light for processing foods. IUVA News 8, 24e28.
Krisko, A., Radman, M., 2010. Protein damage and death by radiation in Escherichia
coli and Deinococcus radiodurans. PNAS (USA) 107 (32), 14373e14377.
Leslie, T., Whitehouse, C., Yingst, S., Baldwin, C., Kakar, F., Moflen, J., Hami, A.,
Mustafah, L., Omar, F., Ayazi, E., Rossi, C., Noormad, B., Ziar, N., Kakar, R., 2010.
Outbreak of gastroenteritis caused by Yersinia pestis in Afghanisatan. Epidemiol.
Infect. 139, 1e8.
Paoli, G., Sommers, C., 2014. Inactivation of avirulent pgmþ and Dpgm Yersinia
pestis by ultraviolet light (UV-C). Food Microbiol. 44, 168e172.
Porto-Fett, A., Juneja, V., Tamplin, M., Luchansky, J., 2009. Validation of cooking
times and temperatures for thermal inactivation of Yersinia pestis strains KIM5
and CDC-A1122 in irradiated ground beef. J. Food Prot. 72 (3), 564e571.
Rajkowski, K., Sommers, C., 2012. Effect of trisodium phosphate or water dip on the
survival of Salmonella and Listeria monocytogenes inoculated catfish before and
after freezing. J. Aquat. Food Product. Technol. 1 (1), 39e47.
Rose, L., O'Connell, H., 2009. UV light inactivation of bacterial biothreat agents. Appl.
Environ. Microbiol. 75, 2987e2990.
Reardon, J., Sancar, A., 2005. Nucleotide excision repair. Prog. Nucleic Acid Res. Mol.
Biol. 79, 183e235.
Rutala, W., Gergen, M., Weber, D., 2010. Room decontamination with UV radiation.
Infect. Control Hosp. Epidemiol. 31, 1025e1029.
Salvage, B., 2014. Strengthening Meat Safety. MeatPoultry.com: The business jour-
nal for Meat and poultry processors. Available at: http://www.meatpoultry.
com/Writers/Bryan%20Salvage/Strengthening%20meat%20safety.aspx?cck¼1
(accessed 23.07.14.).
Sommers, C., Gunther, N., 2013. Inactivation of Campylobacter jejuni on poultry by
ultraviolet light. In: Proceedings, 2013 Midwest Poultry Forum. St. Paul Riv-
erCentre, St. Paul, MN, pp. 1e4.
Sommers, C., Scullen, B., Paoli, G., Bhaduri, S., 2012. Inactivation of Francisella
tularensis Utah-112 on food and food contact surfaces by ultraviolet light.
J. Food Process. Technol. http://dx.doi.org/10.4172/2157-7110.S11-002.
Sommers, C., Rajkowski, K., Sheen, S., Samer, C., Bender, E., 2011. The effect of
cryogenic freezing and gamma irradiation on the survival of Salmonella on
frozen shrimp. J. Food Process. Technol. http://dx.doi.org/10.4172/2157-
7110.S8eS001.
Sommers, C., Sites, J., Musgrove, M., 2010. Ultraviolet light (254 nm) inactivation of
pathogens on foods and stainless steel surfaces. J. Food Saf. 30, 70e79.
Sommers, C., Cooke, P., 2009. Inactivation of avirulent Yersinia pestis in butterfield's
phosphate buffer and frankfurters by UVC (254 nm) and gamma radiation.
J. Food Prot. 72, 755e759.
Sommers, C., Niemira, B., 2007. Effect of temperature on the radiation resistance of
Yersinia pestis suspended in raw ground pork. J. Food Saf. 27, 317e325.
Sumner, S., Wallner-Pendleton, E., Froning, G., Stetson, L., 1996. Inhibition of Sal-
monella typhimurium on agar medium and poultry skin by ultraviolet energy.
J. Food Prot. 59, 319e321.
Stermer, R., Lasater-Smith, M., Brasington, C., 1987. Ultraviolet radiation-an effective
bactericide for fresh meat. J. Food Prot. 50, 108e111.
Torosian, S., Regan, P., Doran, T., Taylor, M., Margolin, A., 2009. A refrigeration
temperature of 4
C does not prevent static growth of Yersinia pestis in heart
infusion broth. Can. J. Microbiol. 55, 1119e1124.
World Health Organization (WHO), 1970. Tularemia. In: Health Aspects of Chemical
and Biological Weapons. World Health Organization, Geneva, SUI, pp. 105e107.