Effect of non-thermal processing techniques on pathogenic and spoilage microorganisms of milk and milk products

SHABBIR, Muhmmad Asim; AHMED, Haassan; MAAN, Abid Aslam; REHMAN, Abdur; AFRAZ, Muhammad Talha; IQBAL, Muhammad Waheed; KHAN, Imran Mehmood; AMIR, Rai Muhammad; ASHRAF, Waqas; KHAN, Moazzam Rafiq; AADIL, Rana Muhammad

doi:10.1590/fst.05820

Muhmmad Asim SHABBIR

National Institute of Food Science and Technology, University of Agriculture, Faisalabad, Pakistan

Haassan AHMED

National Institute of Food Science and Technology, University of Agriculture, Faisalabad, Pakistan

Abid Aslam MAAN

National Institute of Food Science and Technology, University of Agriculture, Faisalabad, Pakistan

Department of Food Engineering, University of Agriculture, Faisalabad, Pakistan

Abdur REHMAN

State Key Laboratory of Food Science and Technology, Jiangnan University, Jiangsu Wuxi, China

Muhammad Talha AFRAZ

National Institute of Food Science and Technology, University of Agriculture, Faisalabad, Pakistan

Muhammad Waheed IQBAL

State Key Laboratory of Food Science and Technology, Jiangnan University, Jiangsu Wuxi, China

Imran Mehmood KHAN

State Key Laboratory of Food Science and Technology, Jiangnan University, Jiangsu Wuxi, China

http://orcid.org/0000-0002-5752-6834

Rai Muhammad AMIR

Institute of Food and Nutritional Sciences, PMAS Arid Agriculture University, Rawalpindi, Pakistan

Waqas ASHRAF

State Key Laboratory of Food Science and Technology, Jiangnan University, Jiangsu Wuxi, China

Moazzam Rafiq KHAN ^**Corresponding author: mrkhan_ft@yahoo.com

National Institute of Food Science and Technology, University of Agriculture, Faisalabad, Pakistan

Rana Muhammad AADIL

National Institute of Food Science and Technology, University of Agriculture, Faisalabad, Pakistan

http://orcid.org/0000-0002-0185-0096

*Corresponding author: mrkhan_ft@yahoo.com

Microorganisms	Dairy Food	Treatment conditions	Reduction	References
B. stearothermophilus ATCC 7953	Skim milk	84 °C at 300 MPa	0.67-log	Pinho et al. (2011)Pinho, C. R., Franchi, M. A., Tribst, A. A., & Cristianinia, M. (2011). Effect of high pressure homogenization process on Bacillus stearothermophilus and Clostridium sporogenes spores in skim milk. Procedia Food Science, 1, 869-873.
C. sporogenes PA 3679	Skim milk	84 °C at 300 MPa	0.67-log
Bacillus spores	Commercial sterile milk	300 MPa at 75-85 °C	~5-log CFU/mL	Amador Espejo et al. (2014)Amador Espejo, G. G., Hernández-Herrero, M. M., Juan, B., & Trujillo, A. J. (2014). Inactivation of Bacillus spores inoculated in milk by ultra high pressure homogenization. Food Microbiology, 44, 204-210. http://dx.doi.org/10.1016/j.fm.2014.06.010. PMid:25084664. http://dx.doi.org/10.1016/j.fm.2014.06.0...
S. typhimurium	Milk	K (1/min) = 0.768, 350 MPa	3 min D value	Patterson et al. (1995)Patterson, M. F., Quinn, M., Simpson, R., & Gilmour, A. (1995). Sensitivity of vegetative pathogens to high hydrostatic pressure treatment in phosphate-buffered saline and foods. Journal of Food Protection, 58(5), 524-529. http://dx.doi.org/10.4315/0362-028X-58.5.524. PMid:31137263. http://dx.doi.org/10.4315/0362-028X-58.5...
Y. enterocolitica		K (1/min) = 0.768, 275 MPa	3 min D value	Patterson et al. (1995)Patterson, M. F., Quinn, M., Simpson, R., & Gilmour, A. (1995). Sensitivity of vegetative pathogens to high hydrostatic pressure treatment in phosphate-buffered saline and foods. Journal of Food Protection, 58(5), 524-529. http://dx.doi.org/10.4315/0362-028X-58.5.524. PMid:31137263. http://dx.doi.org/10.4315/0362-028X-58.5...
E. coli		K (1/min) = 2.303, 400 MPa, Temp. = 50 °C	1 min D value	Gervilla et al. (1997)Gervilla, R., Felipe, X., Ferragut, V., & Guamis, B. (1997). Effect of high hydrostatic pressure on Escherichia coli and Pseudomonas fluorescens strains in bovine milk. Journal of Dairy Science, 80, 2297-2303.
E. coli O157:H7		K (1/min) = 0.768, 400 MPa, Temp. = 50 °C	3 min D value	Patterson & Kilpatrick (1998)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. http://dx.doi.org/10.4315/0362-028X-61.4.432. PMid:9709206. http://dx.doi.org/10.4315/0362-028X-61.4...
S. aureus		K (1/min) = 0.92, 500 MPa, Temp. = 50 °C	2.5 min D value
L. monocytogenes		K (1/min) = 0.768, 375 MPa	3 min D value	Patterson et al. (1995)Patterson, M. F., Quinn, M., Simpson, R., & Gilmour, A. (1995). Sensitivity of vegetative pathogens to high hydrostatic pressure treatment in phosphate-buffered saline and foods. Journal of Food Protection, 58(5), 524-529. http://dx.doi.org/10.4315/0362-028X-58.5.524. PMid:31137263. http://dx.doi.org/10.4315/0362-028X-58.5...
P. fluorescens		K (1/min) = 2.303, 300 MPa, Temp. = 50 °C	1 min D value	Gervilla et al. (1997)Gervilla, R., Felipe, X., Ferragut, V., & Guamis, B. (1997). Effect of high hydrostatic pressure on Escherichia coli and Pseudomonas fluorescens strains in bovine milk. Journal of Dairy Science, 80, 2297-2303.
P. fluorescens		K (1/min) = 3.838, 345 MPa Temp. =50 °C	0.6 min D value	Kalchayanand et al. (1998)Kalchayanand, N., Sikes, A., Dunne, C., & Ray, B. (1998). Factors influencing death and injury of foodborne pathogens by hydrostatic pressure-pasteurization. Food Microbiology, 15(2), 207-214. http://dx.doi.org/10.1006/fmic.1997.0155. http://dx.doi.org/10.1006/fmic.1997.0155...
S. typhimurium	Raw milk	25 °C, 300 MPa	9.21 min D value	Erkmen, (2009)Erkmen, O. (2009). Mathematical modeling of Salmonella typhimurium inactivation under high hydrostatic pressure at different temperatures. Food and Bioproducts Processing, 87(1), 68-73. http://dx.doi.org/10.1016/j.fbp.2008.05.002. http://dx.doi.org/10.1016/j.fbp.2008.05....
C. sporogenes	Milk	90 °C, 700 MPa	13.6 min D value	Shao & Ramaswamy, (2011)Shao, Y., & Ramaswamy, H. S. (2011). Clostridium sporogenes-ATCC 7955 spore destruction kinetics in milk under high pressure and elevated temperature treatment conditions. Food and Bioprocess Technology, 4(3), 458-468. http://dx.doi.org/10.1007/s11947-008-0165-8. http://dx.doi.org/10.1007/s11947-008-016...
E. coli MG1655	Raw milk with 15% fat	300 MPa, 25 °C	3.50-log	Diels et al. (2005)Diels, A. M., Callewaert, L., Wuytack, E. Y., Masschalck, B., & Michiels, C. W. (2005). Inactivation of Escherichia coli by high-pressure homogenisation is influenced by fluid viscosity but not by water activity and product composition. International Journal of Food Microbiology, 101(3), 281-291. http://dx.doi.org/10.1016/j.ijfoodmicro.2004.11.011. PMid:15925711. http://dx.doi.org/10.1016/j.ijfoodmicro....
L. innocua		300 MPa, 24 °C	1.80-log	Picart et al. (2006)Picart, L., Thiebaud, M., René, M., Pierre Guiraud, J., Cheftel, J. C., & Dumay, E. (2006). Effects of high pressure homogenisation of raw bovine milk on alkaline phosphatase and microbial inactivation: a comparison with continuous short-time thermal treatments. The Journal of Dairy Research, 73(4), 454-463. http://dx.doi.org/10.1017/S0022029906001853. PMid:16834813. http://dx.doi.org/10.1017/S0022029906001...
L. monocytogenes		100 MPa, 2-4 °C	1.20-log	Iucci et al. (2007)Iucci, L., Patrignani, F., Vallicelli, M., Guerzoni, M. E., & Lanciotti, R. (2007). Effects of high pressure homogenization on the activity of lysozyme and lactoferrin against Listeria monocytogenes. Food Control, 18, 558-565.
S. aureus		300 MPa, 20 °C	4.00-log	Briñez et al. (2007)Briñez, W. J., Roig-Sagués, A. X., Herrero, M. M. H., & López, B. G. (2007). Inactivation of Staphylococcus ssp. Strains in whole milk and orange juice using ultra high pressure homogenization at inlet temperatures of 6 and 20ºC. Food Control, 18, 1282-1288.

Microorganisms	Dairy food	Treatment conditions	Reduction	References
E. coli	Milk submitted to ultrafiltration	50 pulses of 60 kV/cm or 80 pulses of 70 kV/cm	6 and 9-log	Qin et al. (1998)Qin, B.-L., Barbosa-Canovas, G. V., Swanson, B. G., Pedrow, P. D., & Olsen, R. G. (1998). Inactivating microorganisms using a pulsed electric field continuous treatment system. IEEE Transactions on Industry Applications, 34(1), 43-50. http://dx.doi.org/10.1109/28.658715. http://dx.doi.org/10.1109/28.658715...
L. innocua	Pasteurized skim milk	200 µs at 50 kV/cm	2.6-2.7-log	Fernández-Molina (2001)Fernández-Molina, J. J. (2001). Inactivation of Listeria innocua and Pseudomonas fluorescens in skim milk treated with pulsed electric fields. In G. V. Barbosa-Ca’novas & Q. H. Zhang (Eds.), Pulsed electric fields in food processing. Fundamental aspects and applications (pp. 149–166). Lancaster, PA: Technomic Publishing Company Inc.
E. coli K12	Raw bovine milk	89 µs at 40 kV/cm at 32.5 °C	5-log	Cregenzán-Alberti et al. (2015)Cregenzán-Alberti, O., Halpin, R. M., Whyte, P., Lyng, J. G., & Noci, F. (2015). Study of the suitability of the central composite design to predict the inactivation kinetics by pulsed electric fields (PEF) in Escherichia coli, Staphylococcus aureus and Pseudomonas 1048 fluorescens in milk. Food and Bioproducts Processing, 95, 313-322.
S. aureus	Raw bovine milk	89 µs at 40 kV/cm at 32.5 °C	5.2-log
E. Coli	Raw whole milk	25 kV/cm for 200 µs	2.1-log	Zhao et al. (2013)Zhao, W., Yang, R., Shen, X., Zhang, S., & Chen, X. (2013). Lethal and sublethal injury and kinetics of Escherichia coli, Listeria monocytogenes and Staphylococcus aureus in milk by pulsed electric fields. Food Control, 32(1), 6-12. http://dx.doi.org/10.1016/j.foodcont.2012.11.029. http://dx.doi.org/10.1016/j.foodcont.201...
L. monocytogenes	Raw whole milk UHT milk	30 kV/cm after 200 µs	5-log	Zhao et al. (2013)Zhao, W., Yang, R., Shen, X., Zhang, S., & Chen, X. (2013). Lethal and sublethal injury and kinetics of Escherichia coli, Listeria monocytogenes and Staphylococcus aureus in milk by pulsed electric fields. Food Control, 32(1), 6-12. http://dx.doi.org/10.1016/j.foodcont.2012.11.029. http://dx.doi.org/10.1016/j.foodcont.201... Sobrino-López & Martin-Belloso (2006)Sobrino-López, A., & Martin-Belloso, O. (2006). Enhancing inactivation of Staphylococcus aureus in skim milk by combining high-intensity pulsed electric fields and nisin. Journal of Food Protection, 69(2), 345-353. http://dx.doi.org/10.4315/0362-028X-69.2.345. PMid:16496575. http://dx.doi.org/10.4315/0362-028X-69.2...
S. aureus	Raw whole milk UHT milk	150 bipolar pulses of 8 µs at 35 kV/cm	4.5-log
L. innocua	Raw skim milk	2 µ sec, 100 pulses, 50 kV/cm at ambient temperature	2.4-log	Calderon-Miranda (1998)Miranda, M. L. C. (1998). Inactivation of Listeria innocua by pulsed electric fields and nisin. Washington: Washington State University.
E. coli	UHT milk	15 pulses, 22 kV/cm	3-log	Grahl et al. (1992)Grahl, T., Sitzmann, W., & Maèrkl, H. (1992). Killing of microorganisms in fluid media by high-voltage pulses. In DECHEMA Biotechnology Conferences. Weinheim: VCH.
E. coli	Stimulated milk ultrafiltrate	36 kV/cm, 50 pulses	6-log	Qin et al. (1998)Qin, B.-L., Barbosa-Canovas, G. V., Swanson, B. G., Pedrow, P. D., & Olsen, R. G. (1998). Inactivating microorganisms using a pulsed electric field continuous treatment system. IEEE Transactions on Industry Applications, 34(1), 43-50. http://dx.doi.org/10.1109/28.658715. http://dx.doi.org/10.1109/28.658715...
L. innocua	Raw skim milk	15 to 28 °C, 0.5 L/min 100 pulses, 50 kV/cm 0.5 µF, 2 µsec, 3.5 Hz Exponential decay	2.6-log	Fernández-Molina et al. (1999a)Fernández-Molina, J. J., Barkstrom, E., & Torstensson, P. (1999a). Inactivation of Listeria innocua and Pseudomonas fluorescens in skim milk treated with pulsed electric fields (PEF). New York: American Institute of Chemical Engineers.
E. coli	Skim milk	15 ± 1 °C, 4.0 V/µm, 3 µsec, 64 Pulses	3-log	Zhang et al. (1994)Zhang, Q. H., Qin, B. L., Barbosa-Canovas, G. V., & Swanson, B. G. (1994). Inactivation of E. coli for food pasteurization by high-strength pulsed electric fields. Journal of Food Processing and Preservation, 19, 103-118.
E. coli	Stimulated milk ultrafiltrate	< 30 °C, 1.6 (1.2, 1.4, 1.6 tested) V/µm, 200-300 µsec, 60 (20, 30, 40, 50, 60) pulses	4-log	Pothakamury et al. (1995)Pothakamury, U. R., Monsalve-Gonzalez, A., Barbosa-Cánovas, G. V., & Swanson, B. G. (1995). Inactivation of Escherichia coli and Staphylococcus aureus in model foods by pulsed electric field technology. Food Research International, 28(2), 167-171.
E. coli	SMUF	< 30 °C, 2.5 V/µm, ± 300 pulses, exponential decay pulse width 20 µsec	7-log	Qin et al. (1995)Qin, B.-L., Chang, F.-J., Barbosa-Cánovas, G. V., & Swanson, B. G. (1995). Nonthermal inactivation of Saccharomyces cerevisiae in apple juice using pulsed electric fields. Lebensmittel-Wissenschaft + Technologie, 28(6), 564-568. http://dx.doi.org/10.1016/0023-6438(95)90002-0. http://dx.doi.org/10.1016/0023-6438(95)9...
L. lactis	Skim milk	35 kV/cm, 90 µs, 22 °C	1-log	Michalac et al. (2003)Michalac, S., Alvarez, V., Ji, T., & Zhang, Q. (2003). Inactivation of selected microorganisms and properties of pulsed electric field processed milk. Journal of Food Processing and Preservation, 27(2), 137-151. http://dx.doi.org/10.1111/j.1745-4549.2003.tb00507.x. http://dx.doi.org/10.1111/j.1745-4549.20...
L. innocua	Milk	40 kV/cm, 50 µs, 10 °C	3.3-log	Noci et al. (2009)Noci, F., Walkling-Ribeiro, M., Cronin, D., Morgan, D., & Lyng, J. (2009). Effect of thermosonication, pulsed electric field and their combination on inactivation of Listeria innocua in milk. International Dairy Journal, 19(1), 30-35. http://dx.doi.org/10.1016/j.idairyj.2008.07.002. http://dx.doi.org/10.1016/j.idairyj.2008...
E. coli	Skim milk	K (x10-2/µs) = 5.14-6.0, 20-45 kV/cm	38.4-44.8 µs D value	Martin et al. (1997)Martin, O., Qin, B., Chang, F., Barbosa‐Cánovas, G., & Swanson, B. (1997). Inactivation of Escherichia coli in skim milk by high intensity pulsed electric fields. Journal of Food Process Engineering, 20(4), 317-336. http://dx.doi.org/10.1111/j.1745-4530.1997.tb00425.x. http://dx.doi.org/10.1111/j.1745-4530.19...
Salmonella Dublin	Skim milk Milk	K (x10^-2/µs) = 0.054-0.52, 15-40 kV/cm, Temp = 15-40 °C	4-42.4 µs D value	Sensoy et al. (1997)Sensoy, I., Zhang, Q. H., & Sastry, S. K. (1997). Inactivation kinetics of Salmonella dublin by pulsed electric field. Journal of Food Process Engineering, 20(5), 367-381. http://dx.doi.org/10.1111/j.1745-4530.1997.tb00428.x. http://dx.doi.org/10.1111/j.1745-4530.19...
L. monocytogenes (Scott A)	Skim milk Milk	K (x10^-2/µs) = 0.012-0.015, 30 kV/cm, Temp = 10-50 °C	150-200 µs D value	Reina et al. (1998)Reina, L. D., Jin, Z. T., Yousef, A. E., & Zhang, Q. H. (1998). Inactivation of Listeria monocytogenes in milk by pulsed electric field. Journal of Food Protection, 61(9), 1203-1206.
L. innocua	Skim milk	K (x10-2/µs) = 2.995, 50 kV/cm, Temp= 15-28 °C	76.9 µs D value	Fernández-Molina et al. (1999a)Fernández-Molina, J. J., Barkstrom, E., & Torstensson, P. (1999a). Inactivation of Listeria innocua and Pseudomonas fluorescens in skim milk treated with pulsed electric fields (PEF). New York: American Institute of Chemical Engineers.
L. delbrueckii	SMUF Raw skim milk (0.2% milkfat)	K (x10-2/µs) = 0.096-0.115, 16 kV/cm Temp, < 30 °C	2000-2400 µs D value	Pothakamury, (1995)Pothakamury, U. R. (1995). High voltage pulsed electric field inactivation of Bacillus subtilis and Lactobacillus delbrueckii. Revista española de ciencia y tecnología de alimentos, 35(1), 101-107.
B. subtilis	SMUF Raw skim milk (0.2% milkfat) Milk	K (x10-2/µs) = 0.077-0.092, 16 kV/cm, Temp < 30 °C	2500-3000 µs D value	Pothakamury, (1995)Pothakamury, U. R. (1995). High voltage pulsed electric field inactivation of Bacillus subtilis and Lactobacillus delbrueckii. Revista española de ciencia y tecnología de alimentos, 35(1), 101-107. Qin et al. (1994)Qin, B. L., Zhang, Q., Barbosa-Cánovas, G. V., Swanson, B. G., & Pedrow, P. D. (1994). Inactivation of microorganisms by pulsed electric fields with different voltage waveforms. EEE Transactions on Dielectrics and Electrical Insulation, 1(6), 1047-1057.
B. subtilis P. fluorescens		K (x10-2/µs) = 0.44-0.54, 16 kV/cm	425-520 µs D value	Pothakamury, (1995)Pothakamury, U. R. (1995). High voltage pulsed electric field inactivation of Bacillus subtilis and Lactobacillus delbrueckii. Revista española de ciencia y tecnología de alimentos, 35(1), 101-107. Qin et al. (1994)Qin, B. L., Zhang, Q., Barbosa-Cánovas, G. V., Swanson, B. G., & Pedrow, P. D. (1994). Inactivation of microorganisms by pulsed electric fields with different voltage waveforms. EEE Transactions on Dielectrics and Electrical Insulation, 1(6), 1047-1057. Fernández-Molina et al. (1999b)Fernández-Molina, J., Barkstrom, E., Torstensson, P., Barbosa-Cánovas, G., & Swanson, B. (1999b). Shelf-life extension of raw skim milk by combining heat and pulsed electric fields. In G. V. Barbosa-Cánovas & S. Lombardo (Eds.), The 6th Conference of Food Engineering. Dallas: AIChE.
B. subtilis P. fluorescens S. Dublin		15-28 °C, 0.51/min 30 pulses, 50 kV/cm, 0.5 µF, 2 µsec, 4.0 Hz Exponential decay	2.7-log
B. subtilis P. fluorescens S. Dublin		63 °C, 3.67 V/µm, 36 µsec, 40 pulses	4.0-log	Dunn & Pearlman (1987)Dunn, J. E., & Pearlman, J. S. (1987). U.S. Patent 4,695,472. Methods and apparatus for extending the shelf-life of fluid food products. San Diego, CA: Maxwell Laboratories, Inc.
Lactobacillus brevis	Yogurt	(50 °C, 1.8 V/µm	2.0-log	Dunn & Pearlman (1987)Dunn, J. E., & Pearlman, J. S. (1987). U.S. Patent 4,695,472. Methods and apparatus for extending the shelf-life of fluid food products. San Diego, CA: Maxwell Laboratories, Inc.
B. stearothermophilus	3.4% fat milk	60 kV/cm, 200µs, 50 °C (T_in)	3-log	Shin et al. (2007)Shin, J. K., Jung, K. J., Pyun, Y. R., & Chung, M. S. (2007). Application of pulsed electric fields with square wave pulse to milk inoculated with E. coli, P. fluorescens, and B. stearothermophilus. Food Science and Biotechnology, 16, 1082-1084.
L. lactis	Skim milk	35 kV/cm, 90 µs, 22 °C	1-log	Michalac et al. (2003)Michalac, S., Alvarez, V., Ji, T., & Zhang, Q. (2003). Inactivation of selected microorganisms and properties of pulsed electric field processed milk. Journal of Food Processing and Preservation, 27(2), 137-151. http://dx.doi.org/10.1111/j.1745-4549.2003.tb00507.x. http://dx.doi.org/10.1111/j.1745-4549.20...
P. fluorescens	3.4% fat milk	60 kV/cm, 200 µs, 40 °C (T_in)	5-log	Shin et al. (2007)Shin, J. K., Jung, K. J., Pyun, Y. R., & Chung, M. S. (2007). Application of pulsed electric fields with square wave pulse to milk inoculated with E. coli, P. fluorescens, and B. stearothermophilus. Food Science and Biotechnology, 16, 1082-1084.
Cronobacter sakazakii	Infant formula milk	35 kV/cm, 500µs, 5 °C (T_in)	1.2-log	Pina-Perez et al. (2009)Pina-Perez, M. C., Rodrigo, D., & Lopez, A. M. (2009). Sub-lethal damage in Cronobacter sakazakii subsp sakazakii cells after different pulsed electric field treatments in infant formula milk. Food Control, 20, 1145-1150.
L. innocua	3.6% Fat whole milk	29 kV/cm, 250 µs, < 45 °C	1.5-2-log	Picart et al. (2002)Picart, L., Dumay, E., & Cheftel, J. C. (2002). Inactivation of Listeria innocua in dairy fluids by pulsed electric fields: influence of electric parameters and food composition. Innovative Food Science & Emerging Technologies, 3, 357-369.
Mycobacterium paratuberculosis	Milk	30 kV/cm, 2500 pulses, ~50 °C	5.6-log, 5.9-log	Rowan et al. (2001)Rowan, N. J., MacGregor, S. J., Anderson, J. G., Cameron, D., & Farish, O. (2001). Inactivation of Mycobacterium paratuberculosis by pulsed electric fields. Applied and Environmental Microbiology, 67, 2833-2836.
L. innocua	Whole milk	40 kV/cm, 43.75 µs, 68 °C	5.5-log	Guerrero-Beltrán et al. (2010)Guerrero-Beltrán, J. Á., Sepulveda, D. R., Góngora-Nieto, M. M., Swanson, B., & Barbosa-Cánovas, G. (2010). Milk thermization by pulsed electric fields (PEF) and electrically induced heat. Journal of Food Engineering, 100(1), 56-60. http://dx.doi.org/10.1016/j.jfoodeng.2010.03.027. http://dx.doi.org/10.1016/j.jfoodeng.201...
S. aureus	Skim milk	25 kV/cm, 100 µs, ~50 °C	3-log	Sobrino-López & Martín-Belloso (2008)Sobrino-López, A., & Martín-Belloso, O. (2008). Enhancing the lethal effect of high intensity pulsed electric field in milk by antimicrobial compounds as combined hurdles. Journal of Dairy Science, 91, 1759-1768.

Microorganisms	Dairy Food	Treatment conditions	Reduction	References
E. coli	Raw whole 4% fat cow’s milk	20 kHz, 120 µm,12 min, 60 °C	3.1-log	Herceg et al. (2012)Herceg, Z., Režek Jambrak, A., Lelas, V., & Mededovic Thagard, S. (2012). The effect of high intensity ultrasound treatment on the amount of Staphylococcus aureus and Escherichia coli in milk. Food Technology and Biotechnology, 50(1), 46-52.
E. coli	Raw milk (pasteurization)	20 kHz, 10 min, 750 W	5.34-log CFU/g	Cameron et al. (2009)Cameron, M., McMaster, L. D., & Britz, T. J. (2009). Impact of ultrasound on dairy spoilage microbes and milk components. Dairy Science & Technology, 89(1), 83-98. http://dx.doi.org/10.1051/dst/2008037. http://dx.doi.org/10.1051/dst/2008037...
P. fluorescens		20 kHz, 6 min, 750 W	5.64-log CFU/g
L. monocytogenes		20 kHz, 10 min, 750 W	2.07-log CFU/g
L. monocytogenes	UHT milk	Heat at 60 °C with Sonication at 20 kHz	D_60&S = 0.3 min	Earnshaw et al. (1995)Earnshaw, R., Appleyard, J., & Hurst, R. (1995). Understanding physical inactivation processes: combined preservation opportunities using heat, ultrasound and pressure. International Journal of Food Microbiology, 28(2), 197-219. http://dx.doi.org/10.1016/0168-1605(95)00057-7. PMid:8750667. http://dx.doi.org/10.1016/0168-1605(95)0...
S. typhimurium	Skim milk	30 min at 50 °C 30 min at 40 °C	3-log 2.5-log	Wrigley and Llorca (1992)Wrigley, D. M., & Llorca, N. G. (1992). Decrease of Salmonella typhimurium in skim milk and egg by heat and ultrasonic wave treatment. Journal of Food Protection, 55(9), 678-680. http://dx.doi.org/10.4315/0362-028X-55.9.678. PMid:31084132. http://dx.doi.org/10.4315/0362-028X-55.9...
E. coli K12DH5 Α	UHT milk (pH 6.7)	110 µm, 60 °C	D_60&S = 23s	Zenker et al. (2003)Zenker, M., Heinz, V., & Knorr, D. (2003). Application of ultrasound assisted thermal processing for preservation and quality retention of liquid foods. Journal of Food Protection, 66, 1642-1649.

Microorganisms	Dairy Food	Treatment conditions	Reduction	References
L. monocytogenes	Goat milk	15.8 ± 1.6 mJ/cm², 18 s	5-log	Matak et al. (2005)Matak, K., Churey, J., Worobo, R., Sumner, S., Hovingh, E., Hackney, C., & Pierson, M. (2005). Efficacy of UV light for the reduction of Listeria monocytogenes in goat’s milk. Journal of Food Protection, 68(10), 2212-2216. http://dx.doi.org/10.4315/0362-028X-68.10.2212. PMid:16245732. http://dx.doi.org/10.4315/0362-028X-68.1...
E. coli ATCC 25922	Skim milk (0%fat)	5.8 mJ/cm² for 1.5 sec, 4 °C	2.29-log	Bandla (2010)Bandla, S. (2010). Design of Dean flow ultraviolet (UV) reactors and testing their efficacy for inactivation of Escherichia coli W and Bacillus cereus spores in milk. Carbondale: Southern Illinois University.
	Reduced fat milk (2%fat)		1.82-log
	Whole milk (3.25%fat)		0.73-log
E. coli	Soya milk	Dean flow reactor (1.6 mm), µv dose (0.05 J/mL)	> 5-log	Bandla et al. (2012)Bandla, S., Choudhary, R., Watson, D. G., & Haddock, J. (2012). UV-C treatment of soymilk in coiled tube UV reactors for inactivation of Escherichia coli W1485 and Bacillus cereus endospores. Lebensmittel-Wissenschaft + Technologie, 46(1), 71-76. http://dx.doi.org/10.1016/j.lwt.2011.10.024. http://dx.doi.org/10.1016/j.lwt.2011.10....
	Raw cow milk		4-log
	Skimmed milk		> 7-log

Microorganisms	Dairy Food	Treatment conditions	Reduction	References
E. coli O157:H7 ATCC43895	Milk	35-40 kV, exit temperature < 60 °C, single pass CHIEF	≥ 3.94-log	Ruan (2007)Ruan, R. R. (2007). Concentrated High Intensity Electric Field (CHIEF) technology for liquid food pasteurization. In IFT Annual Meeting. Chicago: Institute of Food Technologists.
Salmonella (5 strain mixture)	Skim milk		2.95-log
L. monocytogenes (5 strain mixture)			2.74-log
B. cereus (3 strain mixture)			0.18-log
E. coli O157:H7 (5 strain mixture)		35-40 kV, exit temperature < 60 °C, double pass CHIEF	4.36-log
Salmonella (5 strain mixture)			5.55-log
L. monocytogenes (5 strain mixture)			4.73-log

Microorganisms	Dairy Food	Treatment conditions	Reduction	References
E. coli ATCC 25922	Whole milk	9 kV of AC power supply, 20 min, temp below 35 °C	3.63-log	Korachi et al. (2010)Korachi, M., Gurol, C., & Aslan, N. (2010). Atmospheric plasma discharge sterilization effects on whole cell fatty acid profiles of Escherichia coli and Staphylococcus aureus. Journal of Electrostatics, 68(6), 508-512. http://dx.doi.org/10.1016/j.elstat.2010.06.014. http://dx.doi.org/10.1016/j.elstat.2010.... ; Korachi & Aslan, (2011)Korachi, M., & Aslan, N. (2011). The effect of atmospheric pressure plasma corona discharge on pH, lipid content and DNA of bacterial cells. Plasma Science & Technology, 13(1), 99-105. http://dx.doi.org/10.1088/1009-0630/13/1/20. http://dx.doi.org/10.1088/1009-0630/13/1...
	Semi-skimmed milk		3.40-log
	Skimmed milk		3.34-log

Microorganisms	Dairy Food	Treatment conditions	Reduction	References
Total bacterial load	Skim milk	MF-1.4 μm, ceramic membrane, Tp = 50 °C	5.18-log	Awad et al. (2010)Awad, S., Ahmed, N., & El Soda, M. (2010). Influence of microfiltration and adjunct culture on quality of domiati cheese. Journal of Dairy Science, 93(5), 1807-1814.
	Reconstituted skim milk	MF-1.4 μm, ceramic membrane, Tp = 50 °C	4.5-log	Pafylias et al. (1996)Pafylias, I., Cheryan, M., Mehaia, M., & Saglam, N. (1996). Microfiltration of milk with ceramic membranes. Food Research International, 29(2), 141-146. http://dx.doi.org/10.1016/0963-9969(96)00007-5. http://dx.doi.org/10.1016/0963-9969(96)0...
	Skim milk	MF-1.4 μm, ceramic membrane, Tp = 55 °C	>3.5-log	Maubois (2002)Maubois, J. (2002). Membrane microfiltration: a tool for a new approach in dairy technology. Australian Journal of Dairy Technology, 57(2), 92.
Spore forming bacteria		MF-1.4 μm	>4.5-log	Trouvé et al. (1991)Trouvé, E., Maubois, J. L., Piot, M., Madec, M. N., Fauquant, J., Rouault, A., Tabard, J., & Brinkman, G. (1991). Retention of various microbial species during milk purification by cross-flow microfiltration. Le Lait, 72, 327-332.
Spores		MF-1.4 μm, ceramic membrane, Tp = 55 °C	>4.5-log	Maubois (2002)Maubois, J. (2002). Membrane microfiltration: a tool for a new approach in dairy technology. Australian Journal of Dairy Technology, 57(2), 92.
Bacillus cereus spores		MF-1.4 μm, ceramic membrane	3.5-log	Olesen & Jensen (1989)Olesen, N., & Jensen, F. (1989). Microfiltration - the influence of operation parameters on the process. Milchwissenschaft. Milk Science International, 44(8), 476-479.
Bacillus subtilis	Simulated milk ultrafiltrate	MF-0.5 μm (micro sieve)	6.6-log	Brans et al. (2004)Brans, G., Schroën, C., Van der Sman, R., & Boom, R. (2004). Membrane fractionation of milk: state of the art and challenges. Journal of Membrane Science, 243(1-2), 263-272. http://dx.doi.org/10.1016/j.memsci.2004.06.029. http://dx.doi.org/10.1016/j.memsci.2004....
Total bacterial load	Skim milk	MF-0.8 μm, tubular ceramic ISOFLUX® membrane	>2.3-log	Gosch et al. (2014)Gosch, T., Apprich, S., Kneifel, W., & Novalin, S. (2014). A combination of microfiltration and high pressure treatment for the elimination of bacteria in bovine colostrum. International Dairy Journal, 34(1), 41-46. http://dx.doi.org/10.1016/j.idairyj.2013.06.014. http://dx.doi.org/10.1016/j.idairyj.2013...

Treatment	Microorganisms	Dairy food	Treatment conditions	Reduction	References
Thermosonication	S. aureus	Milk 4% fat	20 kHz, 4,8 min, 120 µm, 60 °C	1-log CFU/g	Herceg et al. (2012)Herceg, Z., Režek Jambrak, A., Lelas, V., & Mededovic Thagard, S. (2012). The effect of high intensity ultrasound treatment on the amount of Staphylococcus aureus and Escherichia coli in milk. Food Technology and Biotechnology, 50(1), 46-52.
	L. innocua	Raw and whole cow’s milk	63 ± 0.5 °C, 24 kHz, 129 mW/mL, 400 W, 120 mm, 10 min	5-log CFU/mL	Bermúdez-Aguirre et al. (2011)Bermúdez-Aguirre, D., Mawson, R., & Barbosa-Canovas, G. B. (2011). Study of possible mechanisms of inactivation of Listaeria Innocua in thermo-sonicated milk using scanning electron microscopy and trasmission electron microscopy. Journal of Food Processing and Preservation, 35, 767-777.
	E. coli	Milk 4% fat	20 kHz, 2.78 min	1-log CFU/g	Herceg et al. (2012)Herceg, Z., Režek Jambrak, A., Lelas, V., & Mededovic Thagard, S. (2012). The effect of high intensity ultrasound treatment on the amount of Staphylococcus aureus and Escherichia coli in milk. Food Technology and Biotechnology, 50(1), 46-52.
PEF and electrically induced heat	L. innocua	Pasteurized whole milk	40 kV/cm, 15 pulses, 23 °C (T_i), 10 s	5.5-log	Guerrero-Beltrán et al. (2010)Guerrero-Beltrán, J. Á., Sepulveda, D. R., Góngora-Nieto, M. M., Swanson, B., & Barbosa-Cánovas, G. (2010). Milk thermization by pulsed electric fields (PEF) and electrically induced heat. Journal of Food Engineering, 100(1), 56-60. http://dx.doi.org/10.1016/j.jfoodeng.2010.03.027. http://dx.doi.org/10.1016/j.jfoodeng.201...
Thermosonication	L. innocua	Raw whole milk	120 µm, 2.85 W/cm²/63 ± 0.5 °C/30 min	3.58-log	Earnshaw, Appleyard and Hurst, (1995)Earnshaw, R., Appleyard, J., & Hurst, R. (1995). Understanding physical inactivation processes: combined preservation opportunities using heat, ultrasound and pressure. International Journal of Food Microbiology, 28(2), 197-219. http://dx.doi.org/10.1016/0168-1605(95)00057-7. PMid:8750667. http://dx.doi.org/10.1016/0168-1605(95)0...
	B. subtilis spores	Whole milk	US: 20 kHz,150 W, V=30 mL, 100 °C	D_{TUS =} 1.6	García et al. (1989)García, M. L., Burgos, J., Sanz, B., & Ordonez, J. (1989). Effect of heat and ultrasonic waves on the survival of two strains of Bacillus subtilis. The Journal of Applied Bacteriology, 67(6), 619-628. PMid:2515184.
	L. monocytogenes	UHT milk	US: 20 kHz, 150 W, V = 30 mL, 60 °C	D_{TUS =} 0.3
	E. coli	UHT milk (pH 6.7)	US: 20 kHz, 110 μm, V = 10 mL, 60 °C	D_{TUS =} 0.4	Zenker et al. (2003)Zenker, M., Heinz, V., & Knorr, D. (2003). Application of ultrasound assisted thermal processing for preservation and quality retention of liquid foods. Journal of Food Protection, 66, 1642-1649.
HPP and Heat	L. monocytogenes	UHT milk	375 MPA/15 min/35 °C	3.5-log	Simpson & Gilmour (1997)Simpson, R., & Gilmour, A. (1997). The resistance of Listeria monocytogenesto high hydrostatic pressure in foods. Food Microbiology, 14(6), 567-573. http://dx.doi.org/10.1006/fmic.1997.0117. http://dx.doi.org/10.1006/fmic.1997.0117...
HPP and Heat	E. coli O157:H7	UHT milk	400 MPA/15 min/50 °C	5.0-log	Patterson & Kilpatrick (1998)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. http://dx.doi.org/10.4315/0362-028X-61.4.432. PMid:9709206. http://dx.doi.org/10.4315/0362-028X-61.4...

[1] *Corresponding author: mrkhan_ft@yahoo.com

Brasil

Brasil

Effect of non-thermal processing techniques on pathogenic and spoilage microorganisms of milk and milk products

Abstract