High Pressure Processing of Foods for Microbial and Mycotoxins Control: current trends and future prospects

Figures & data

Table 1. Microbial inactivation by HPP in different food products

Food product	Target microorganism	Pressure	Temperature	Holding time	Reduction	Reference
Maize	Fusarium graminearum	380 MPa	60 °C	30 min	100%	Kalagatur et al. (2018)
Black olive oils	Total mold	250 MPa	25 °C	5 min	90%	Tokuşoğlu et al. (2010)
		250 MPa	4 °C	5 min	100%
Milk	C. perfringens	600 MPa	65 °C	12.5 min	2.54-log	Gao, Qiu, Wu, and Fu (2011)
Milk	C. perfringens	900 MPa	100 °C	5 min	4-log	Shao, Zhu, Ramaswamy, and Marcotte (2010)
Milk buffer	Bacillus cereus spores	600 MPa	80 °C	20 min	7.53-log	Ju, Gao, Yao, and Qian (2008)
Egg patties	B. stearothermophilus	700 MPa	105 °C	5 min	4-log	Rajan, Pandrangi, Balasubramaniam, and Yousef (2006)
Beef broth	B. stearothermophilus	600 MPa	105 °C	5 min	3-log	Devatkal, Somerville, Thammakulkrajang, and Balasubramaniam (2015)
Tomato sauce	A. acidoterrestris and B. coagulans	600 MPa	60 °C		3.5 and 2.0-log, respectively	Vercammen et al. (2012)
Beef slurry	C. perfringens	600 MPa	75 °C	20 min	2.2-log	Evelyn and Silva (2017)
Milk	B. cereus spores	600 MPa	70 °C	20 min	4-log
Apple juice	Neosartorya fischeri	600 MPa	75 °C	20 min	4.3-log
Strawberry puree	B. nivea	600 MPa	75 °C	20 min	2-log
Cheese	Penicillium roqueforti	400 MPa	10 °C	20 min	>2-log	O’Reilly, O’Connor, Kelly, Beresford, and Murphy (2000)
	Penicillium roqueforti	400 MPa	20 and 30 °C	20 min	6-log
	S. aureus	>600 MPa	20 °C		Complete inactivation
	E. coli	400 MPa	30 °C	20 min	Complete inactivation
Milk	E. coli	400 MPa	50 °C	15 min	5–6 log	Patterson and Kilpatrick (1998)
Apple juice	L. monocytogenes, S. aureus, E. coli, S. tiphimurium, S. cerevisiae	500 MPa	25 °C	1 min	4.8, 2.4, 5.0, 7.0 5.8, respectively	Shahbaz et al. (2016)
Cactus juice	Viable microbial cells, Yeast/Molds Acid tolerant microorganims	600 MPa	15 °C	10 min	3 log	Moussa-Ayoub et al. (2017)
Cantaloupe puree	Total aerobic bacteria	300–500 MPa	8, 15 °C	5 min	1–3.3 log	Mukhopadhyay, Sokorai, Ukuku, Fan, and Juneja (2017)
Soy smoothies	Aerobic mesophilic bacteria	450–650 MPa	20 °C	3 min	3 log	Andrés, Villanueva, and Tenorio (2016)
Banana smoothie	Yeasts/Molds	550 MPa	20 °C	2–10 min	2.5 log	Li, Wang, Wang, and Liao (2015)
Keiskei juice	Yeasts/Molds	550 MPa	Room temperature	1.5 min	4.8 log	Chai, Lee, Lee, Na, and Park (2014)
Mango nectar	Total aerobic bacteria	600 MPa	20 °C	1 min	5.2 log	Liu, Li, Wang, Bi, and Liao (2014)

Figure 1. Chemical structure of patulin.

Table 2. Mycotoxins control by HPP in different food products

Food product	Mycotoxin	Pressure	Holding time	Temperature (°C)	Reduction	Reference
Apple juice	Patulin (PAT)	30–500 MPa	300 s	30–50	56.24%	Avsaroglu et al. (2015)
GJ* blend juice	Patulin (PAT)	600 MPa	300 s	11 °C	62 ppb	Hao et al. (2016)
Apple juice	Patulin	300, 400 and 500 MPa	5 min	20, 30, 40	62.11%	Avsaroglu et al. (2015)
Maize	Deoxynivalenol (DON), zearalenone (Zea)	550 MPa	20 min	45	Complete inactivation	Kalagatur et al. (2018)
Black olive oils	citrinin	250 MPa	5 min	35 ± 2	64–100%	Tokuşoğlu et al. (2010)

*GJ blend juice is prepared from romaine, celery, cucumber, apple, spinach, kale, parsley and lemon.

Table 3. Combinations of HPP and moderate temperatures to reach an inactivation of at least 5 log10 cycles in different pathogenic vegetative microorganisms

Microorganisms	Media	Treatment	T (°C)	Inactivation (log10)	Reference
L. monocytogenes NCTC 11,994	UHT milk	375 MPa/15 min	45	>7.0	Simpson and Gilmour (1997)
E. coli O157:H7 12,079	Poultry meat	400 MPa/15 min	50	6.0	Patterson and Kilpatrick (1998)
	UHT milk	400 MPa/15 min	50	5.0
S. aureus 10,652	Poultry meat	400 MPa/15 min	50	5.0
	UHT milk	500 MPa/15 min	50	6.0
S. aureus 582	0.1% Peptone	276 MPa/15 min	35	6.5	Kalchayanand et al. (1998)
			45	7.7
			50	>8.7
L. monocytogenes Scott A	0.1% Peptone	276 MPa/15 min	45	6.4
			50	>8.0
S. typhimurium ATCC 14,082	0.1% Peptone	276 MPa/15 min	25	5.5
			35	>7.8
E. coli O157:H7	0.1% Peptone	276 MPa/15 min	45	>7.7
L. monocytogenes CA	1% Peptone	345 MPa/15 min	50	>8.1	Alpas et al. (1999)
L. monocytogenes ohio2	1% Peptone	345 MPa/15 min	50	>8.0
S. aureus 485	1% Peptone	345 MPa/15 min	50	5.4
S. aureus 765	1% Peptone	345 MPa/15 min	50	>8.1
E. coli O157:H7 933	1% Peptone	345 MPa/15 min	50	>8.3
E. coli O157:H7 931	1% Peptone	345 MPa/15 min	50	>8.2
S. enteritidis FDA	1% Peptone	345 MPa/15 min	50	>8.2
S. typhimurium E21274	1% Peptone	345 MPa/15 min	50	>8.4

Figure 2. Possible effects obtained by combining different preservation technologies.

Table 4. Combinations of HPP and moderate temperatures to reach an inactivation of at least 5 log10 cycles in different bacterial spores

Microorganisms	Media	Treatment	T (°C)	Inactivation (log10)	Reference
B. coagulans NCTC 3991	Sodium phosphate buffer (pH 8)	400 MPa/30 min	55	5.0	Sale, Gould, and Hamilton (1970)
			65	7.0
B. stearothermophilus IFO 12,550	Not reported	600 MPa/6 cycles of 5 min	70	6.0	Hayakawa et al. (1994)
B. cereus	Phosphate buffer (pH 7)	700 MPa/5 min	50	>5.0	Fornari, Maggi, Gola, Cassara, and Manachini (1995)
			60	>5.0
			70	>5.0
B. licheniformis	Phosphate buffer (pH 7)	700 MPa/5 min	60	5.0
			70	>6.5
B. stearothermophilus	Phosphate buffer (pH 7)	700 MPa/5 min	70	5.0
B. cereus ATCC 14,579 sporulated at 30 °C	Mcllvaine buffer (pH 7)	700 MPa/15 min	40	6.0	Raso et al. (1998b)
		400 MPa/15 min	60	6.0
C. botulinum type E (Alaska)	Sorensen buffer (pH 7)	827 MPa/5 min	55	5.0	Reddy et al. (1999)
C. botulinum type E (Beluga)			50	5.0
B. stearothermophilus ATCC 7953	Mashed broccoli	600 MPa/60 min	80	6.0	Ananta, Heinz, Schlüter, and Knorr (2001)
		600 MPa/30 min	90	6.0
		400 MPa/45 min	95	6.0
		500 MPa/30 min		6.0

Kalagatur, N. K., Kamasani, J. R., Mudili, V., Krishna, K., Chauhan, O. P., & Sreepathi, M. H. (2018). Effect of high pressure processing on growth and mycotoxin production of Fusarium graminearum in maize. Food Bioscience, 21, 53–59. doi:10.1016/j.fbio.2017.11.005

 Web of Science ®Google Scholar

Tokuşoğlu, Ö., Alpas, H., & Bozoğlu, F. (2010). High hydrostatic pressure effects on mold flora, citrinin mycotoxin, hydroxytyrosol, oleuropein phenolics and antioxidant activity of black table olives. Innovative Food Science & Emerging Technologies, 11(2), 250–258. doi:10.1016/j.ifset.2009.11.005

 Web of Science ®Google Scholar

Gao, Y., Qiu, W., Wu, D., & Fu, Q. (2011). Assessment of Clostridium perfringens spore response to high hydrostatic pressure and heat with nisin. Applied Biochemistry and Biotechnology, 164(7), 1083–1095. doi:10.1007/s12010-011-9196-0

 PubMed Web of Science ®Google Scholar

Shao, Y., Zhu, S., Ramaswamy, H., & Marcotte, M. (2010). Compression heating and temperature control for high-pressure destruction of bacterial spores: An experimental method for kinetics evaluation. Food and Bioprocess Technology, 3(1), 71. doi:10.1007/s11947-008-0057-y

 Web of Science ®Google Scholar

Ju, X.-R., Gao, Y.-L., Yao, M.-L., & Qian, Y. (2008). Response of Bacillus cereus spores to high hydrostatic pressure and moderate heat. LWT-Food Science and Technology, 41(10), 2104–2112. doi:10.1016/j.lwt.2007.11.011

 Web of Science ®Google Scholar

Rajan, S., Pandrangi, S., Balasubramaniam, V., & Yousef, A. E. (2006). Inactivation of Bacillus stearothermophilus spores in egg patties by pressure-assisted thermal processing. LWT-Food Science and Technology, 39(8), 844–851. doi:10.1016/j.lwt.2005.06.008

 Web of Science ®Google Scholar

Devatkal, S., Somerville, J., Thammakulkrajang, R., & Balasubramaniam, V. (2015). Microbiological efficacy of pressure assisted thermal processing and natural extracts against Bacillus amyloliquefaciens spores suspended in deionized water and beef broth. Food and Bioproducts Processing, 95, 183–191. doi:10.1016/j.fbp.2015.05.007

 Web of Science ®Google Scholar

Vercammen, A., Vivijs, B., Lurquin, I., & Michiels, C. W. (2012). Germination and inactivation of Bacillus coagulans and Alicyclobacillus acidoterrestris spores by high hydrostatic pressure treatment in buffer and tomato sauce. International Journal of Food Microbiology, 152(3), 162–167. doi:10.1016/j.ijfoodmicro.2011.02.019

 PubMed Web of Science ®Google Scholar

Evelyn, M. E., & Silva, F. V. M. (2017). Comparing high pressure thermal processing and thermosonication with thermal processing for the inactivation of bacteria, moulds, and yeasts spores in foods. Journal of Food Engineering, 214, 90–96. doi:10.1016/j.jfoodeng.2017.06.027

 Web of Science ®Google Scholar

O’Reilly, C. E., O’Connor, P. M., Kelly, A. L., Beresford, T. P., & Murphy, P. M. (2000). Use of hydrostatic pressure for inactivation of microbial contaminants in cheese. Applied and Environmental Microbiology, 66(11), 4890–4896. doi:10.1128/aem.66.11.4890-4896.2000

 PubMed Web of Science ®Google Scholar

Patterson, M. F., & Kilpatrick, D. J. (1998). The combined effect of high hydrostatic pressure and mild heat on inactivation of pathogens in milk and poultry. Journal of Food Protection, 61(4), 432–436.

 PubMed Web of Science ®Google Scholar

Shahbaz, H. M., Yoo, S., Seo, B., Ghafoor, K., Kim, J. U., Lee, D.-U., & Park, J. (2016). Combination of TiO 2-UV photocatalysis and high hydrostatic pressure to inactivate bacterial pathogens and yeast in commercial apple juice. Food and Bioprocess Technology, 9(1), 182–190. doi:10.1007/s11947-015-1614-9

 Web of Science ®Google Scholar

Moussa-Ayoub, T. E., Jäger, H., Knorr, D., El-Samahy, S. K., Kroh, L. W., & Rohn, S. (2017). Impact of pulsed electric fields, high hydrostatic pressure, and thermal pasteurization on selected characteristics of Opuntia dillenii cactus juice. LWT-Food Science and Technology, 79, 534–542. doi:10.1016/j.lwt.2016.10.061

 Web of Science ®Google Scholar

Mukhopadhyay, S., Sokorai, K., Ukuku, D., Fan, X., & Juneja, V. (2017). Effect of high hydrostatic pressure processing on the background microbial loads and quality of cantaloupe puree. Food Research International, 91, 55–62. doi:10.1016/j.foodres.2016.11.029

 PubMed Web of Science ®Google Scholar

Andrés, V., Villanueva, M.-J., & Tenorio, M.-D. (2016). Influence of high pressure processing on microbial shelf life, sensory profile, soluble sugars, organic acids, and mineral content of milk-and soy-smoothies. LWT-Food Science and Technology, 65, 98–105. doi:10.1016/j.lwt.2015.07.066

 Web of Science ®Google Scholar

Li, R., Wang, Y., Wang, S., & Liao, X. (2015). A comparative study of changes in microbiological quality and physicochemical properties of N 2-infused and N 2-degassed banana smoothies after high pressure processing. Food and Bioprocess Technology, 8(2), 333–342. doi:10.1007/s11947-014-1401-z

 Web of Science ®Google Scholar

Chai, C., Lee, J., Lee, Y., Na, S., & Park, J. (2014). A combination of TiO2–UV photocatalysis and high hydrostatic pressure to inactivate Bacillus cereus in freshly squeezed Angelica keiskei juice. LWT-Food Science and Technology, 55(1), 104–109. doi:10.1016/j.lwt.2013.08.015

 Web of Science ®Google Scholar

Liu, F., Li, R., Wang, Y., Bi, X., & Liao, X. (2014). Effects of high hydrostatic pressure and high-temperature short-time on mango nectars: Changes in microorganisms, acid invertase, 5-hydroxymethylfurfural, sugars, viscosity, and cloud. Innovative Food Science & Emerging Technologies, 22, 22–30. doi:10.1016/j.ifset.2013.11.014

 Web of Science ®Google Scholar

Avsaroglu, M., Bozoglu, F., Alpas, H., Largeteau, A., & Demazeau, G. (2015). Use of pulsed-high hydrostatic pressure treatment to decrease patulin in apple juice. High Pressure Research, 35(2), 214–222. doi:10.1080/08957959.2015.1027700

 Web of Science ®Google Scholar

Hao, H., Zhou, T., Koutchma, T., Wu, F., & Warriner, K. (2016). High hydrostatic pressure assisted degradation of patulin in fruit and vegetable juice blends. Food Control, 62, 237–242. doi:10.1016/j.foodcont.2015.10.042

 Web of Science ®Google Scholar

Simpson, R., & Gilmour, A. (1997). The resistance of Listeria monocytogenes to high hydrostatic pressure in foods. Food Microbiology, 14(6), 567–573. doi:10.1006/fmic.1997.0117

 Web of Science ®Google Scholar

Kalchayanand, N., Sikes, A., Dunne, C., & Ray, B. (1998). Interaction of hydrostatic pressure, time and temperature of pressurization and pediocin AcH on inactivation of foodborne bacteria. Journal of Food Protection, 61(4), 425–431.

 PubMed Web of Science ®Google Scholar

Alpas, H., Kalchayanand, N., Bozoglu, F., Sikes, A., Dunne, C., & Ray, B. (1999). Variation in resistance to hydrostatic pressure among strains of food-borne pathogens. Applied and Environmental Microbiology, 65(9), 4248–4251.

 PubMed Web of Science ®Google Scholar

Sale, A., Gould, G., & Hamilton, W. (1970). Inactivation of bacterial spores by hydrostatic pressure. Microbiology, 60(3), 323–334.

 Google Scholar

Hayakawa, I., Kanno, T., Yoshiyama, K., & Fujio, Y. (1994). Oscillatory compared with continuous high pressure sterilization on Bacillus stearothermophilus spores. Journal of Food Science, 59(1), 164–167. doi:10.1111/jfds.1994.59.issue-1

 Web of Science ®Google Scholar

Fornari, C., Maggi, A., Gola, S., Cassara, A., & Manachini, P. L. (1995). Inactivation of Bacillus endospores by high-pressure treatment. Industria Conserve, 70(3), 259–265.

 Google Scholar

Raso, J., Calderón, M. L., Góngora, M., Barbosa‐Cánovas, G. V., & Swanson, B. G. (1998b). Inactivation of Zygosaccharomyces bailii in fruit juices by heat, high hydrostatic pressure and pulsed electric fields. Journal of Food Science, 63(6), 1042–1044. doi:10.1111/j.1365-2621.1998.tb15850.x

 Web of Science ®Google Scholar

Reddy, N., Solomon, H., Fingerhut, G., Rhodehamel, E., Balasubramaniam, V., & Palaniappan, S. (1999). Inactivation of Clostridium botulinum type E spores by high pressure processing. Journal of Food Safety, 19(4), 277–288. doi:10.1111/jfs.1999.19.issue-4

 Web of Science ®Google Scholar

Ananta, E., Heinz, V., Schlüter, O., & Knorr, D. (2001). Kinetic studies on high-pressure inactivation of Bacillus stearothermophilus spores suspended in food matrices. Innovative Food Science & Emerging Technologies, 2(4), 261–272. doi:10.1016/S1466-8564(01)00046-7

 Google Scholar