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Campylobacter heat resistance - past, current status and future prospect for New Zealand and beyond

Published online by Cambridge University Press:  10 March 2015

A. AL-SAKKAF
A. AL-SAKKAF*
Affiliation:
Institute of Food, Nutrition and Human Health, Massey University, Riddet Road, Palmerston North 4474, New Zealand
*
Corresponding author: AlsakkafAli@gmail.com
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Abstract

New Zealand has a much higher rate of reported campylobacteriosis cases than the rest of the developed world. It has been assumed that New Zealand C. jejuni strains have greater heat tolerance and thus are better able to survive cooking. Therefore there is a need to fully determine the temperature dependence of Campylobacter spp. and to update the current knowledge of kinetic parameters such as D and z values of Campylobacter spp. The significantly higher reported D- values for Campylobacter spp. already seen in the Netherlands requires a practical stance in ensuring appropriate evaluation of thermal process lethality of Campylobacter spp. An extensive search of data bases for publications on Campylobacter heat resistance was conducted. The kinetic parameters obtained in New Zealand under isothermal and dynamic conditions in broths or in food matrix are broadly in agreement with previously published international data and do not indicate that New Zealand strains are more heat resistant than other strains. This finding has a significant impact to regulators, consumers, food industry and researchers as it has revealed the scientific evidence to maintain the standards for the heat treatment practices. Any change of heat treatment practice can cause unpredicted loss to the poultry industry and challenges the regulatory bodies to convey the message of altering the consumers cooking temperature to all consumers with a short time given the reluctance of consumers in using thermometers to verify the cooking temperature at home. Consumers play an important role in making certain the food they prepare is safe by preventing cross-contamination in order to avoid the risk of food borne diseases.

Keywords

Campylobacterheat resistancetemperatureD and z valuesinactivation
Type
Reviews
Information
World's Poultry Science Journal , Volume 71 , Issue 1 , March 2015 , pp. 111 - 124
Copyright
Copyright © World's Poultry Science Association 2015 

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References

ACUFF, G.R., VANDERZANT, C., HANNA, M.O., EHLERS, J.B. and GARDNER, F.A. (1986) Effects of handling and preparation of turkey products on the survival of campylobacter jejuni. Journal of Food Protection 49: 627-631.CrossRefGoogle ScholarPubMed
ADAMS, M.R. and MOSS, M.O. (2000) Food microbiology (Cambridge, Royal Society of Chemistry).Google Scholar
AL-SAKKAF, A. (2012) Evaluation of food handling practice among new zealanders and other developed countries as a main risk factor for campylobacteriosis rate. Food Control 27: 330-337.Google Scholar
AL-SAKKAF, A. (2013a) Campylobacteriosis in New Zealand: A new twist to the tale? Part one (the pathogen and the poultry plant). Food Control 33: 556-561.Google Scholar
AL-SAKKAF, A. (2013b) Domestic food preparation practices: A review of the reasons for poor home hygiene practices. Health Promotion International: doi: 10.1093/heapro/dat051.Google Scholar
AL-SAKKAF, A. and JONES, G. (2012) Thermal inactivation of campylobacter jejuni in broth. Journal of Food Protection 75: 1029-1035.Google Scholar
AL-SAKKAF, A., JONES, G. and MAWSON, J. (2010) Survival of New Zealand relevant campylobacter strains final report: N0174/06 prepared for nzfsa available on line http://www.Foodsafety.Govt.Nz/elibrary/industry/campylobacter-strains/index.Htm.Google Scholar
AL-SAKKAF, A. and MAWSON, J. (2009) Thermal inactivation of campylobacter jejuni on chicken skin (Niigata, Japan, 15th International Workshop on Campylobacter, Helicobacter, and related organisms).Google Scholar
ALTER, T. and SCHERER, K. (2006) Stress response of campylobacter spp. And its role in food processing. Journal of Veterinary Medicine Series B 53: 351-357.Google Scholar
BARRELL, R.A.E. (1984) The survival of campylobacter jejuni in red meats stored at different temperatures. International Journal of Food Microbiology 1: 187-196.Google Scholar
BERGEY, D.H., BOONE, D.R., CASTENHOLZ, R.W., BRENNER, D.J., KRIEG, N.R., STALEY, J.T. and GARRITY, G.M. (2001) Bergey's manual of systematic bacteriology (New York, Springer).Google Scholar
BERGSMA, N.J., FISCHER, A.R.H., VAN ASSELT, E.D., ZWIETERING, M.H. and DE JONG, A.E.I. (2007) Consumer food preparation and its implication for survival of campylobacter jejuni on chicken. British Food Journal 109: 548-561.Google Scholar
BLANKENSHIP, L.C. and CRAVEN, S.E. (1982) Campylobacter jejuni survival in chicken meat as a function of temperature. Applied and Environmental Microbiology 44: 88-92.CrossRefGoogle ScholarPubMed
BOLTON, F.J., HUTCHINSON, D.N. and COATES, D. (1984) Blood-free selective medium for isolation of campylobacter jejuni from feces. Journal of Clinical Microbiology 19: 169-171.CrossRefGoogle ScholarPubMed
BOSTAN, K. (2001) Effects of cooking and cold storage on the survival of campylobacter jejuni in meatballs. Archiv Fur Lebensmittelhygiene 52: 28-30.Google Scholar
BRACEWELL, A.J., REAGAN, J.O., CARPENTER, J.A. and BLANKENSHIP, L.C. (1985) Factors affecting survival of campylobacter jejuni on experimentally inoculated pork skin stored under various conditions. Journal of Food Protection 48: 944-946.Google Scholar
BROWN, M.E. (1988) Introduction to thermal analysis : Techniques and applications (London; New York, Chapman and Hall).Google Scholar
BUSWELL, C.M., HERLIHY, Y.M., LAWRENCE, L.M., MCGUIGGAN, J.T., MARSH, P.D., KEEVIL, C.W. and LEACH, S.A. (1998) Extended survival and persistence of campylobacter spp. In water and aquatic biofilms and their detection by immunofluorescent-antibody and -rrna staining. Applied and Environmental Microbiology 64: 733-741.Google Scholar
CFSAN (2008) The bad bug book: Foodborne pathogenic microorganisms and natural toxins handbook (College Park, Md., US Food and Drug Administration, Center for Food Safety and Applied Nutrition).Google Scholar
CHAN, K.F., TRAN, H.L., KANENAKA, R.Y. and KATHARIOU, S. (2001) Survival of clinical and poultry-derived isolates of campylobacter jejuni at a low temperature (4 degrees c). Applied and Environmental Microbiology 67: 4186-4191.Google Scholar
CHRISTOPHER, F.M., SMITH, G.C. and VANDERZANT, C. (1982) Effect of temperature and ph on the survival of campylobacter fetus. Journal of Food Protection 45: 253-259.Google Scholar
CHUNG, H.J., BIRLA, S.L. and TANG, J. (2008) Performance evaluation of aluminum test cell designed for determining the heat resistance of bacterial spores in foods. LWT - Food Science and Technology 41: 1351-1359.Google Scholar
COGAN, T.A., SLADER, J., BLOOMFIELD, S.F. and HUMPHREY, T.J. (2002) Achieving hygiene in the domestic kitchen: The effectiveness of commonly used cleaning procedures. Journal of Applied Microbiology 92: 885-892.CrossRefGoogle ScholarPubMed
COLE, M.B. and JONES, M.V. (1990) A submerged-coil heating apparatus for investigating thermal inactivation of micro-organisms. Letters in Applied Microbiology 11: 233-235.CrossRefGoogle Scholar
CONDON, S., ARRIZUBIETA, M.J. and SALA, F.J. (1993) Microbial heat resistance determinations by the multipoint system with the thermoresistometer tr-sc. Improvement of this methodology. Journal of Microbiological Methods 18: 357-366.Google Scholar
CONDON, S., LOPEZ, P., ORIA, R. and SALA, F.J. (1989) Thermal death determination: Design and evaluation of a thermoresistometer. Journal of Food Science 54: 451-457.CrossRefGoogle Scholar
CONESA, R., ANDREU, S., FERNANDEZ, P.S., ESNOZ, A. and PALOP, A. (2009) Nonisothermal heat resistance determinations with the thermoresistometer mastia. Journal of Applied Microbiology 107: 506-513.Google Scholar
COOLS, I., UYTTENDAELE, M., CARO, C., D'HAESE, E., NELIS, H.J. and DEBEVERE, J. (2003) Survival of campylobacter jejuni strains of different origin in drinking water. Journal of Applied Microbiology 94: 886-892.Google Scholar
CORRY, J.E., POST, D.E., COLIN, P. and LAISNEY, M.J. (1995) Culture media for the isolation of campylobacters. International Journal of Food Microbiology 26: 43-76.Google Scholar
CORRY, J.E.L., JAMES, S.J., PURNELL, G., BARBEDO-PINTO, C.S., CHOCHOIS, Y., HOWELL, M. and JAMES, C. (2007) Surface pasteurisation of chicken carcasses using hot water. Journal of Food Engineering 79: 913-919.Google Scholar
COX, N.A., RICHARDSON, L.J., BAILEY, J.S., COSBY, D.E., CASON, J.A., MUSGROVE, M.T. and MEAD, G.C. (2005) Bacterial contamination of poultry as a risk to human health (CRC Press).Google Scholar
DE CESARE, A., SHELDON, B.W., SMITH, K.S. and JAYKUS, L.A. (2003) Survival and persistence of campylobacter and salmonella species under various organic loads on food contact surfaces. Journal of Food Protection 66: 1587-1594.CrossRefGoogle ScholarPubMed
DE JONG, A.E.I., VAN ASSELT, E.D., ZWIETERING, M.H., NAUTA, M.J. and DE JONGE, R. (2008) Extreme heat resistence of campylobacter jejuni, escherichia coli, and salmonella typhimurium during cooking of chicken breast fillet. The 21st International ICFMH Symposium: 170.Google Scholar
DINGLE, K.E., COLLES, F.M., WAREING, D.R.A., URE, R., FOX, A.J., BOLTON, F.E., BOOTSMA, H.J., WILLEMS, R.J.L., URWIN, R. and MAIDEN, M.C.J. (2001) Multilocus sequence typing system for campylobacter jejuni. Journal of Clinical Microbiology 39: 14-23.Google Scholar
DONNISON, A. (2002) Isolation of thermotolerant campylobacter – review & methods for New Zealand laboratories (Prepared for the Ministry of Health under the auspices of the Enteric Zoonotic Disease Research in New Zealand Steering Committee).Google Scholar
DOWNES, F. and ITO, K. (2001) Compendium of methods for the microbiological examination of foods (Washington, American Public Health Association).Google Scholar
DOYLE, M.P. and ROMAN, D.J. (1981) Growth and survival of campylobacter fetus subsp. Jejuni as a function of temperature and ph. Journal of Food Protection 44: 596-601.Google Scholar
ELSGAARD, L. and JØRGENSEN, L.W. (2002) A sandwich-designed temperature-gradient incubator for studies of microbial temperature responses. Journal of Microbiological Methods 49: 19-29.Google Scholar
ENRIGHT, M.C. and SPRATT, B.G. (1999) Multilocus sequence typing. Trends in Microbiology 7: 482-487.Google Scholar
FDA/CFSAN (2000) Kinetics of microbial inactivation for alternative food processing technologies (Food & Drug Administration, Center for Food Safety and Applied Nutrition).Google Scholar
FORSYTHE, S.J. (2000) The microbiology of safe food (Oxford; Malden, MA, Blackwell Science).Google Scholar
FOSTER, A.M., KETTERINGHAM, L.P., SWAIN, M.J., KONDJOYAN, A., HAVET, M., ROUAUD, O. and EVANS, J.A. (2006) Design and development of apparatus to provide repeatable surface temperature-time treatments on inoculated food samples. Journal of Food Engineering 76: 7-18.Google Scholar
FRENCH, N. (2008a) Enhancing surveillance of potentially foodborne enteric diseases in New Zealand: Human campylobacteriosis in the manawatu (Wellington, FDI / 236 /2005 Massey University, report for New Zealand Food Safety Authority (NZFSA)).Google Scholar
FRENCH, N. (2008b) Human campylobacteriosis in the manawatu. Report for nzfsa (Palmerston North, Massey University).Google Scholar
GARAIZAR, J., REMENTERIA, A. and PORWOLLIK, S. (2006) DNA microarray technology: A new tool for the epidemiological typing of bacterial pathogens? FEMS Immunology & Medical Microbiology 47: 178-189.Google Scholar
GILBERT, S.E., WHYTE, R., BAYNE, G., PAULIN, S.M., LAKE, R.J. and VAN DER LOGT, P. (2007) Survey of domestic food handling practices in New Zealand. International Journal of Food Microbiology 117: 306-311.Google Scholar
GILL, C.O. and HARRIS, L.M. (1982) Survival and growth of campylobacter fetus subsp. Jejuni on meat and in cooked foods. Applied and Environmental Microbiology 44: 259-263.Google Scholar
GRIGORIADIS, S.G., KOIDIS, P.A., VARELTZIS, K.P. and BATZIOS, C.A. (1997) Survival of campylobacter jejuni inoculated in fresh and frozen beef hamburgers stored under various temperatures and atmospheres. Journal of Food Protection 60: 903-907.Google Scholar
GUERIN, M.T., SIR, C., SARGEANT, J.M., WADDELL, L., O'CONNOR, A.M., WILLS, R.W., BAILEY, R.H. and BYRD, J.A. (2010) The change in prevalence of campylobacter on chicken carcasses during processing: A systematic review. Poultry Science 89: 1070-1084.Google Scholar
GUNSEN, U. (2008) Inactivation of campylobacter jejuni inoculated into baked drumsticks. Archiv Fur Lebensmittelhygiene 59: 175-179.Google Scholar
HABIB, I., SAMPERS, I., UYTTENDAELE, M., BERKVENS, D. and DE ZUTTER, L. (2008) Performance characteristics and estimation of measurement uncertainty of three plating procedures for campylobacter enumeration in chicken meat. Food Microbiology 25: 65-74.Google Scholar
HABIB, I., UYTTENDAELE, M. and DE ZUTTER, L. (2010) Survival of poultry-derived campylobacter jejuni of multilocus sequence type clonal complexes 21 and 45 under freeze, chill, oxidative, acid and heat stresses. Food Microbiology 27: 829-834.Google Scholar
HANNINEN, M.L., KORKEALA, H. and PAKKALA, P. (1984) Effect of various gas atmospheres on the growth and survival of campylobacter jejuni on beef. Journal of Applied Bacteriology 57: 89-94.Google Scholar
HAZELEGER, W.C., WOUTERS, J.A., ROMBOUTS, F.M. and ABEE, T. (1998) Physiological activity of campylobacter jejuni far below the minimal growth temperature. Applied and Environmental Microbiology 64: 3917-3922.Google Scholar
HUMPHREY, T., MASON, M. and MARTIN, K. (1995) The isolation of campylobacter jejuni from contaminated surfaces and its survival in diluents. International Journal of Food Microbiology 26: 295-303.Google Scholar
HUMPHREY, T.J. and CRUICKSHANK, J.G. (1985) Antibiotic and deoxycholate resistance in campylobacter jejuni following freezing or heating. Journal of Applied Bacteriology 59: 65-71.Google Scholar
HUMPHREY, T.J. and LANNING, D.G. (1987) Salmonella and campylobacter contamination of broiler chicken carcasses and scald tank water - the influence of water ph. Journal of Applied Bacteriology 63: 21-25.Google Scholar
HUMPHREY, T.J., MARTIN, K.W., SLADER, J. and DURHAM, K. (2001) Campylobacter spp. In the kitchen: Spread and persistence. Journal of Applied Microbiology Symposium Supplement 90: 115S-120S.Google Scholar
ICMSF (1996) Microorganisms in foods 5: Microbiological specifications of food pathogens (London, Chapman and Hall, for the International Commission on Microbiological Specifications for Foods).Google Scholar
JACKOWSKA, A., SZCZAWIŃSKI, J., PE¸CONEK, J. and FONBERG-BROCZEK, M. (2008) Possibility of campylobacter jejuni inactivation in smoked salmon by high-pressure treatment. High Pressure Research: An International Journal 28: 127-132.Google Scholar
JACOBS-REITSMA, W. (2000) Campylobacter in the food supply (Washington DC, American Society for Microbiology).Google Scholar
JASSON, V., UYTTENDAELE, M., RAJKOVIC, A. and DEBEVERE, J. (2007) Establishment of procedures provoking sub-lethal injury of listeria monocytogenes, campylobacter jejuni and escherichia coli o157 to serve method performance testing. International Journal of Food Microbiology 118: 241-249.Google Scholar
JONES, F.S., ORCUTT, M. and LITTLE, R.B. (1931) Vibrios (vibrio jejuni, n. Sp.) associated with intestinal disorders of cows and calves (Rockefeller Univ Press).Google Scholar
JONSSON, M., HEIER, B., NORSTROM, M. and HOFSHAGEN, M. (2010) Analysis of simultaneous space-time clusters of campylobacter spp. In humans and in broiler flocks using a multiple dataset approach. International Journal of Health Geographics 9: 48.Google Scholar
JOSHUA, G.W.P., GUTHRIE-IRONS, C., KARLYSHEV, A.V. and WREN, B.W. (2006) Biofilm formation in campylobacter jejuni. Microbiology-SGM 152: 387-396.Google Scholar
KELLY, A.F., PARK, S.F., BOVILL, R. and MACKEY, B.M. (2001) Survival of campylobacter jejuni during stationary phase: Evidence for the absence of a phenotypic stationary-phase response. Applied and Environmental Microbiology 67: 2248-2254.Google Scholar
KELLY, D.J. (2008) Complexity and versatility in the physiology and metabolism of campylobacter jejuni (Washington, DC, ASM Press).Google Scholar
KETLEY, J.M. (1997) Pathogenesis of enteric infection by campylobacter. Microbiology (UK) 143: 5-21.Google Scholar
KOIDIS, P. and DOYLE, M.P. (1983) Survival of campylobacter-jejuni in fresh and heated red meat. Journal of Food Protection 46: 771-774.CrossRefGoogle ScholarPubMed
LAKE, R., HUDSON, A., CRESSEY, P. and NOTRJE, G. (2003) Risk profile: Campylobacter jejuni /coli in poultry (whole and pieces) (Christchurch, Institute of Environmental Science & Research Limited).Google Scholar
LEE, A., SMITH, S.C. and COLOE, P.J. (1998) Survival and growth of campylobacter jejuni after artificial inoculation onto chicken skin as a function of temperature and packaging conditions. Journal of Food Protection 61: 1609-1614.Google Scholar
LI, Y., YANG, H. and SWEM, B. (2002) Effect of high-temperature inside-outside spray on survival of campylobacter jejuni attached to prechill chicken carcasses. Poultry Science 81: 1371-1377.Google Scholar
LINE, J.E. (2001) Development of a selective differential agar for isolation and enumeration of campylobacter spp. Journal of Food Protection 64: 1711-1715.Google Scholar
LINE, J.E. (2006) Comparison of enrichment vessels for recovery of campylobacter spp. From broiler rinse samples. Journal of Rapid Methods and Automation in Microbiology 14: 110-117.Google Scholar
LORI, S., BUCKOW, R., KNORR, D., HEINZ, V. and LEHMACHERI, A. (2007) Predictive model for inactivation of campylobacter spp. By heat and high hydrostatic pressure. Journal of Food Protection 70: 2023-2029.Google Scholar
MAIDEN, M.C.J., BYGRAVES, J.A., FEIL, E., MORELLI, G., RUSSELL, J.E., URWIN, R., ZHANG, Q., ZHOU, J., ZURTH, K., CAUGANT, D.A., FEAVERS, I.M., ACHTMAN, M. and SPRATT, B.G. (1998) Multilocus sequence typing: A portable approach to the identification of clones within populations of pathogenic microorganisms. Proceedings of the National Academy of Sciences of the United States of America95: 3140-3145.Google Scholar
MARTINEZ-RODRIGUEZ, A., KELLY, A.F., PARK, S.F. and MACKEY, B.M. (2004) Emergence of variants with altered survival properties in stationary phase cultures of campylobacter jejuni. International Journal of Food Microbiology 90: 321-329.Google Scholar
MATTICK, K., DURHAM, K., DOMINGUE, G., JØRGENSEN, F., SEN, M., SCHAFFNER, D.W. and HUMPHREY, T. (2003) The survival of foodborne pathogens during domestic washing-up and subsequent transfer onto washing-up sponges, kitchen surfaces and food. International Journal of Food Microbiology 85: 213-226.Google Scholar
MCKENZIE, A. (2006) Nzfsa moves to curb campylobacter rates (Wellington, New Zealand Food Safety Authority).Google Scholar
MILES, S. and SCAIFE, V. (2003) Optimistic bias and food. Nutrition research reviews 16: 3-19.Google Scholar
MOORE, J.E. and MADDEN, R.H. (2000) The effect of thermal stress on campylobacter coli. Journal of Applied Microbiology 89: 892-899.Google Scholar
MURPHY, C., CARROLL, C. and JORDAN, K.N. (2003) Identification of a novel stress resistance mechanism in campylobacter jejuni. Journal of Applied Microbiology 95: 704-708.Google Scholar
MURPHY, C., CARROLL, C. and JORDAN, K.N. (2005) The effect of different media on the survival and induction of stress responses by campylobacter jejuni. Journal of Microbiological Methods 62: 161-166.Google Scholar
MYLIUS, S.D., NAUTA, M.J. and HAVELAAR, A.H. (2007) Cross-contamination during food preparation: A mechanistic model applied to chicken-borne campylobacter. Risk Analysis 27: 803-813.Google Scholar
NAUTA, M., FISCHER, A.R.H., VAN ASSELT, E.D., DE JONG, A.E.I., FREWER, L.J. and DE JONGE, R. (2008) Food safety in the domestic environment: The effect of consumer risk information on human disease risks. Risk Analysis 28: 179-192.Google Scholar
NEWELL, D.G., SHREEVE, J.E., TOSZEGHY, M., DOMINGUE, G., BULL, S., HUMPHREY, T. and MEAD, G. (2001) Changes in the carriage of campylobacter strains by poultry carcasses during processing in abattoirs. Applied and Environmental Microbiology 67: 2636-2640.Google Scholar
NGUYEN, H.T.T., CORRY, J.E.L. and MILES, C.A. (2006) Heat resistance and mechanism of heat inactivation in thermophilic campylobacters. Applied and Environmental Microbiology 72: 908-913.Google Scholar
NZPHO (2007) Notifiable and other diseases in New Zealand: 2006 (the Institute of Environmental Science and Research).Google Scholar
OOSTEROM, J., WILDE, G.J.A.D., BOER, E.D., BLAAUW, L.H.D. and KARMAN, H. (1983) Survival of campylobacter jejuni during poultry processing and pig slaughtering. Journal of Food Protection 46: 702-706, 709.Google Scholar
PARK, S. (2005) Campylobacter: Stress response and resistance (Cambridge, England, CRC Press, Woodhead).Google Scholar
PARK, S.F. (2002) The physiology of campylobacter species and its relevance to their role as foodborne pathogens. International Journal of Food Microbiology 74: 177-188.Google Scholar
PETERSEN, L., NIELSEN, E.M. and ON, S.L.W. (2001) Serotype and genotype diversity and hatchery transmission of campylobacter jejuni in commercial poultry flocks. Veterinary Microbiology 82: 141-154.Google Scholar
PFLUG, I.J. (1990) Microbiology and engineering of sterilization processes (Minneapolis, MN, Environmental Sterilization Laboratory).Google Scholar
PURNELL, G., MATTICK, K. and HUMPHREY, T. (2004) The use of `hot wash' treatments to reduce the number of pathogenic and spoilage bacteria on raw retail poultry. Journal of Food Engineering 62: 29-36.Google Scholar
ROLLINS, D.M. and COLWELL, R.R. (1986) Viable but nonculturable stage of campylobacter jejuni and its role in survival in the natural aquatic environment. Applied and Environmental Microbiology 52: 531-538.Google Scholar
SAMPERS, I., HABIB, I., DE ZUTTER, L., DUMOULIN, A. and UYTTENDAELE, M. (2010) Survival of campylobacter spp. In poultry meat preparations subjected to freezing, refrigeration, minor salt concentration, and heat treatment. International Journal of Food Microbiology 137: 147-153.Google Scholar
SCHÖNBERG-NORIO, D., SARNA, S., HÄNNINEN, M., KATILA, M., KAUKORANTA, S. and RAUTELIN, H. (2006) Strain and host characteristics of campylobacter jejuni infections in finland. Clinical Microbiology and Infection 12: 754-760.Google Scholar
SEBALD, M. and V'ERON, M. (1963) Base DNA content and classification of vibrios. Annales de l'Institut Pasteur Journal 105: 897-910.Google Scholar
SKIRROW, M.B., BENJAMIN, J., RAZI, M.H.H. and WATERMAN, S. (1982) Isolation, cultivation and identification of Campylobacter jejuni and Campylobacter coli, in: CORRY, J.E.L., ROBERTS, D. & SKINNER, F.A. (Eds) Isolation and Identification Methods for Food Poisoning Organism ( London: Academic Press).Google Scholar
SLAVIK, M.F., KIM, J.W. and WALKER, J.T. (1995) Reduction of salmonella and campylobacter on chicken carcasses by changing scalding temperature. Journal of Food Protection 58: 689-691.Google Scholar
SORQVIST, S. (1989) Heat resistance of campylobacter and yersinia strains by three methods. Journal of Applied Bacteriology 67: 543-549.Google Scholar
SORQVIST, S. (2003) Heat resistance in liquids of enterococcus spp., listeria spp., escherichia coli, yersinia enterocolitica, salmonella spp. And campylobacter spp. Acta Veterinaria Scandinavica 44: 1-19.Google Scholar
STUMBO, C.R. (1973) Thermobacteriology in food processing (New York, Academic Press).Google Scholar
TANG, N. and SCHRAFT, H. (2000) Temperature and mixed-culture effect on campylobacter jejuni biofilm formation (Dallas, TX).Google Scholar
TERZIEVA, S.I. and MCFETERS, G.A. (1991) Survival and injury of escherichia coli, campylobacter jejuni, and yersinia enterocolitica in stream water. Canadian Journal of Microbiology 37: 785-790.Google Scholar
TRACHOO, N. and BROOKS, J.D. (2005) Attachment and heat resistance of campylobacter jejuni on enterococcus faecium biofilm. Pakistan Journal of Biological Sciences 8: 599-605.Google Scholar
VAN ASSELT, E.D. and ZWIETERING, M.H. (2006) A systematic approach to determine global thermal inactivation parameters for various food pathogens. International Journal of Food Microbiology 107: 73-82.Google Scholar
WASSENAAR, T.M. and NEWELL, D.G. (2000) Genotyping of campylobacter spp. Applied and Environmental Microbiology 66: 1-9.Google Scholar
WHYTE, R., HUDSON, J.A. and GRAHAM, C. (2006) Campylobacter in chicken livers and their destruction by pan frying. Letters in Applied Microbiology 43: 591-595.Google Scholar
WINGSTRAND, A., NEIMANN, J., NIELSEN, E.M., GERNER-SMIDT, P., WEGENER, H.C. and MOLBAK, K. (2006) Fresh chicken as main risk factor for campylobacteriosis, Denmark. Emerging Infectious Diseases 12: 280-285.Google Scholar
YANG, H., LI, Y. and JOHNSON, M.G. (2001) Survival and death of salmonella typhimurium and campylobacter jejuni in processing water and on chicken skin during poultry scalding and chilling. Journal of Food Protection 64: 770-776.Google Scholar
ZHAO, T., DOYLE, M.P. and BERG, D.E. (2000) Fate of campylobacter jejuni in butter. Journal of Food Protection 63: 120-122.Google Scholar