Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T10:43:33.940Z Has data issue: false hasContentIssue false
  • English
  • Français

Early blowing in raw goats’ milk cheese: gas production capacity of Enterobacteriaceae species present during manufacturing and ripening

Published online by Cambridge University Press:  08 August 2018

Rafael Tabla ,
Antonia Gómez ,
Alfredo Simancas ,
José Emilio Rebollo ,
Felipe Molina  and
Isidro Roa
Rafael Tabla*
Affiliation:
Dairy Departament, Technological Institute of Food and Agriculture – Scientific and Technological Research Centre of Extremadura (INTAEX – CICYTEX), Junta de Extremadura, Avda. Adolfo Suarez s/n, 06071 Badajoz, Spain
Antonia Gómez
Affiliation:
Dairy Departament, Technological Institute of Food and Agriculture – Scientific and Technological Research Centre of Extremadura (INTAEX – CICYTEX), Junta de Extremadura, Avda. Adolfo Suarez s/n, 06071 Badajoz, Spain
Alfredo Simancas
Affiliation:
Departamento de Bioquímica, Biología Molecular y Genética, Facultad de Ciencias, Universidad de Extremadura, Avda. de Elvas s/n, 06006 Badajoz, Spain
José Emilio Rebollo
Affiliation:
Departamento de Bioquímica, Biología Molecular y Genética, Facultad de Ciencias, Universidad de Extremadura, Avda. de Elvas s/n, 06006 Badajoz, Spain
Felipe Molina
Affiliation:
Departamento de Bioquímica, Biología Molecular y Genética, Facultad de Ciencias, Universidad de Extremadura, Avda. de Elvas s/n, 06006 Badajoz, Spain
Isidro Roa
Affiliation:
Dairy Departament, Technological Institute of Food and Agriculture – Scientific and Technological Research Centre of Extremadura (INTAEX – CICYTEX), Junta de Extremadura, Avda. Adolfo Suarez s/n, 06071 Badajoz, Spain
*
*For correspondence; e-mail: rafael.tabla@juntaex.es
Get access Rights & Permissions [Opens in a new window]

Abstract

The aim of this study was to identify the main Enterobacteriaceae species responsible for early gas blowing during curdling and the first week of ripening in raw goats’ milk cheese. Two batches of raw goats’ milk cheese were selected. One of them showed early blowing within the first 24 h of cheese ripening while the other showed no alteration. Although initial levels of Enterobacteriaceae were similar in defective and non-defective cheese, their dynamics (growth and disappearance rates of the species detected) were different. Klebsiella oxytoca and Enterobacter cloacae were the main species in the defective curd, whereas Buttiauxela spp. was predominant in normal curd. Hafnia alvei was the prevailing isolated species for both normal and defective cheese throughout the ripening process. The highest gas production was rendered by K. oxytoca and H. alvei, mainly isolated from curd and cheese. However, other species relevant in milk or curd, like Pantoea ssp. or Buttiauxela spp. were considered as low gas producers. The analysis of digitalized images of cheese showed that most of the cheese eyes were formed before the first week of ripening, although this process continued during maturation.

According to the species found in the defective and non-defective cheese, their proportions at different ripening stages, their ability to produce gas and eye formation, K. oxytoca might be considered the most likely responsible for early blowing in raw goats’ milk cheeses; while H. alvei increased the eyes number in the later stages of the ripening period.

Keywords

Enterobacteriaceaecheeseraw goat milkripeninggasearly blowing
Type
Research Article
Information
Journal of Dairy Research , Volume 85 , Issue 3 , August 2018 , pp. 331 - 338
Copyright
Copyright © Hannah Dairy Research Foundation 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abriouel, H, Martín-Platero, A, Maqueda, M, Valdivia, E & Martínez-Bueno, M 2008 Biodiversity of the microbial community in a Spanish farmhouse cheese as revealed by culture-dependent and culture-independent methods. International Journal of Food Microbiology 127 200–208Google Scholar
Alichanidis, E 2007 What causes early and late gas blowing in white-brined cheese? In Cheese Problems Solved, pp. 332–335 (Ed. McSweeney, PLH). Abington: Woodhead Publishing LimitedGoogle Scholar
Benkerroum, N 2016 Biogenic amines in dairy products: origin, incidence, and control means. Comprehensive Reviews in Food Science and Food Safety 15 801–826Google Scholar
Bester, BH 1976 Some aspects of gas formation through coliform bacteria in cheese (Enkele aspekte van gasvorming deur kolivormige bakteriee in kaas) South African Journal of Dairy Technology 8 51–55Google Scholar
Bintsis, T & Papademas, P 2002 Microbiological quality of white-brined cheeses: a review. International Journal of Dairy Technology 55 113–120Google Scholar
Brenner, DJ & Farmer, JJ 2005 Family Enterobacteriaceae. In Bergey's Manual of Systematic Bacteriology, Vol. 2B, 2nd edition. pp. 587–606 (Eds Brenner, DJ, Krieg, NR, Staley, JR & Garrity, GM). New York: SpringerGoogle Scholar
Buchin, S, Delague, V, Duboz, G, Berdague, JL, Beuvier, E, Pochet, S & Grappin, R 1998 Influence of pasteurization and fat composition of milk on the volatile compounds and flavor characteristics of a semi-hard cheese. Journal of Dairy Science 81 3097–3108Google Scholar
Delbès-Paus, C, Irlinger, F & Coton, M 2011 Benefits and risks associated with Gram-negative bacteria within cheese microbial communities. 10th International Meeting on Mountain Cheese Ed. University of Turin, DroneroGoogle Scholar
Delbès-Paus, C, Pochet, S, Helinck, S, Veisseire, P, Bord, C, Lebecque, A, Coton, M, Desmasures, N, Coton, E, Irlinger, F & Montel, MC 2012 Impact of Gram-negative bacteria in interaction with a complex microbial consortium on biogenic amine content and sensory characteristics of an uncooked pressed cheese. Food Microbiology 30 74–82Google Scholar
Fox, PF, Guinee, TP, Cogan, TM & McSweeney, PLH 2000 Microbiology of cheese ripening. In Fundamentals of Cheese Science, pp. 206–232 (Ed. Fox, PF). Gaithersburg: Aspen Publishers IncGoogle Scholar
Gaya, P, Medina, M & Núñez, M 1983 Accelerated decrease of Enterobacteriaceae counts during ripening of raw milk Manchego cheese by lactic culture inoculation. Journal of Food Protection 46 305–308Google Scholar
Giannino, ML, Marzotto, M, Dellaglio, F & Feligini, M 2009 Study of microbial diversity in raw milk and fresh curd used for Fontina cheese production by culture-independent methods. International Journal of Food Microbiology 130 188–195Google Scholar
Guggisberg, D, Schuetz, P, Winkler, H, Amrein, R, Jakob, E, Fröhlich-Wyder, MT & Wechsler, D 2015 Mechanism and control of the eye formation in cheese. International Dairy Journal 47 118–127Google Scholar
ISO (International Organization for Standardization), 2004. Cheese and processedcheese − Determination of the total solids content (reference method). ISO5534:2004 (IDF 4: 2004), Geneva, Switzerland.Google Scholar
ISO (International Organization for Standardization), 2006. Cheese and processedcheese products − Determination of chloride content − Potentiometrictitration method. ISO 5943:2006 (IDF 88: 2006), Geneva, Switzerland.Google Scholar
ISO (International Organization for Standardization), 2008. Cheese −Determination of fat content − Van Gulik method. ISO 3433:2008 (IDF 222:2008), Geneva, Switzerland.Google Scholar
Irlinger, F, In Yung, SAY, Sarthou, AS, Delbès-Paus, C, Montel, MC, Coton, E, Coton, M & Helinck, S 2012. Ecological and aromatic impact of twoGram-negative bacteria (Psychrobacter celer and Hafnia alvei) inoculated aspart of the whole microbial community of an experimental smear soft cheese. International Journal of Food Microbioly 153 332–338Google Scholar
Jackman, PJ 1987 Microbial systematics based on electrophoretic whole cell proteins. In Methods in Microbiology, pp. 209–225 (Eds Colwell, RR & Grigorova, R). London: Academic PressGoogle Scholar
Kongo, JM, Gomes, AP & Malcata, FX 2008 Monitoring and identification of bacteria associated with safety concerns in the manufacture of Sao Jorge, a Portuguese traditional cheese from raw cow's milk. Journal of Food Protection 71 986–992Google Scholar
Laemmli, UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680–685Google Scholar
Lück, H & Dunkeld, M 1981 Enterobacteriaceae in cheese. South African Journal of Dairy Technology 13 9–14Google Scholar
Maifreni, M, Frigo, F, Bartolomeoli, I, Innocente, N, Biasutti, M & Marino, M 2013 Identification of the Enterobacteriaceae in Montasio cheese and assessment of their amino acid decarboxylase activity. Journal of Dairy Research 80 122–127Google Scholar
Martley, FG & Crow, VL 1996 Open texture in cheese: the contributions of gas production by microorganisms and cheese manufacturing practices. Journal of Dairy Research 63 489–507Google Scholar
Mas, M, Tabla, R, Moriche, J, Roa, I, Gonzalez, J, Rebollo, JE & Cáceres, P 2002 Ibores goat's milk cheese: microbiological and physicochemical changes throughout ripening. Le Lait 82 579–587Google Scholar
Melilli, C, Barbano, DM, Caccamo, M, Calvo, MA, Schembari, G & Licitra, G 2004 Influence of brine concentration, brine temperature, and presalting on early gas defects in raw milk pasta filata cheese. Journal of Dairy Science 87 3648–3657Google Scholar
Montel, MC, Buchin, S, Mallet, A, Delbes-Paus, C, Vuitton, DA, Desmasures, N & Berthier, F 2014 Traditional cheeses: rich and diverse microbiota with associated benefits. International Journal of Food Microbiology 177 136–154Google Scholar
Official Journal of the European Union, 2004. Publication of an application for registration pursuant to Article 6(2) of Council Regulation (EEC) No 2081/92 on the protection of geographical indications and designations of origin (2004/C 58/07).Google Scholar
Ordiales, E, Benito, MJ, Martín, A, Casquete, R, Serradilla, MJ & de Guía, Córdoba, M 2013 Bacterial communities of the traditional raw ewe's milk cheese “Torta del Casar” made without the addition of a starter. Food Control 33 448–454Google Scholar
Pircher, A, Bauer, F & Paulsen, P 2007 Formation of cadaverine, histamine, putrescine and tyramine by bacteria isolated from meat, fermented sausages and cheeses. European Food Reseach Technology 226 225–231Google Scholar
Psoni, L, Tzanetakis, N & Litopoulou-Tzanetaki, E 2003 Microbiological characteristics of Batzos, a traditional Greek cheese from raw goat's milk. Food Microbiology 20 575–582Google Scholar
Schindelin, J, Arganda-Carreras, I, Frise, E, Kaynig, V, Longair, M, Pietzsch, T & Cardona, A 2012 Fiji: an open-source platform for biological-image analysis. Nature Methods 9 676–682Google Scholar
Sheehan, JJ 2007 What causes the development of gas during ripening? In Cheese Problems Solved, pp. 131–132 (Ed. McSweeney, PLH). Abington: Woodhead Publishing LimitedGoogle Scholar
Tabla, R, Gómez, A, Simancas, A, Rebollo, JE, Molina, F & Roa, I 2016 Enterobacteriaceae species during manufacturing and ripening of semi-hard and soft raw ewe's milk cheese: Gas production capacity. Small Ruminant Research 145 123–129Google Scholar
Tavaria, FK & Malcata, FX 1998 Microbiological characterization of Serra da Estrela cheese throughout its appellation d'Origine Protégée region. Journal of Food Protection 61 601–607Google Scholar
Tornadijo, E, Fresno, JM, Carballo, J & Martín-Sarmiento, R 1993 Study of Enterobacteriaceae throughout the manufacturing and ripening of hard goats'cheese. Journal of Applied Microbiology 75 240–246Google Scholar
Tornadijo, ME, García, MC, Fresno, JM & Carballo, J 2001 Study of Enterobacteriaceae during the manufacture and ripening of San Simón cheese. Food Microbiology 18 499–509Google Scholar
Torracca, B, Pedonese, F, Turchi, B, Fratini, F & Nuvoloni, R 2018 Qualitative and quantitative evaluation of biogenic amines in vitro production by bacteria isolated from ewes’ milk cheeses. European Food Research and Technology 244 721–728Google Scholar
Verdier-Metz, I, Michel, V, Delbès, C & Montel, MC 2009 Do milking practices influence the bacterial diversity of raw milk? Food Microbiology 26 305–310Google Scholar
Westling, M, Danielsson-Tham, ML, Jass, J, Nilsen, A, Öström, Å & Tham, W 2016 Contribution of Enterobacteriaceae to sensory characteristics in soft cheeses made from raw milk. Procedia Food Science 7 17–20Google Scholar