Skip to main content Accessibility help

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

  • Rafael Tabla (a1), Antonia Gómez (a1), Alfredo Simancas (a2), José Emilio Rebollo (a2), Felipe Molina (a2) and Isidro Roa (a1)...


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.


Corresponding author

*For correspondence; e-mail:


Hide All
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 200208
Alichanidis, E 2007 What causes early and late gas blowing in white-brined cheese? In Cheese Problems Solved, pp. 332335 (Ed. McSweeney, PLH). Abington: Woodhead Publishing Limited
Benkerroum, N 2016 Biogenic amines in dairy products: origin, incidence, and control means. Comprehensive Reviews in Food Science and Food Safety 15 801826
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 5155
Bintsis, T & Papademas, P 2002 Microbiological quality of white-brined cheeses: a review. International Journal of Dairy Technology 55 113120
Brenner, DJ & Farmer, JJ 2005 Family Enterobacteriaceae. In Bergey's Manual of Systematic Bacteriology, Vol. 2B, 2nd edition. pp. 587606 (Eds Brenner, DJ, Krieg, NR, Staley, JR & Garrity, GM). New York: Springer
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 30973108
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, Dronero
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 7482
Fox, PF, Guinee, TP, Cogan, TM & McSweeney, PLH 2000 Microbiology of cheese ripening. In Fundamentals of Cheese Science, pp. 206232 (Ed. Fox, PF). Gaithersburg: Aspen Publishers Inc
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 305308
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 188195
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 118127
ISO (International Organization for Standardization), 2004. Cheese and processedcheese − Determination of the total solids content (reference method). ISO5534:2004 (IDF 4: 2004), Geneva, Switzerland.
ISO (International Organization for Standardization), 2006. Cheese and processedcheese products − Determination of chloride content − Potentiometrictitration method. ISO 5943:2006 (IDF 88: 2006), Geneva, Switzerland.
ISO (International Organization for Standardization), 2008. Cheese −Determination of fat content − Van Gulik method. ISO 3433:2008 (IDF 222:2008), Geneva, Switzerland.
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 332338
Jackman, PJ 1987 Microbial systematics based on electrophoretic whole cell proteins. In Methods in Microbiology, pp. 209225 (Eds Colwell, RR & Grigorova, R). London: Academic Press
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 986992
Laemmli, UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680685
Lück, H & Dunkeld, M 1981 Enterobacteriaceae in cheese. South African Journal of Dairy Technology 13 914
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 122127
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 489507
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 579587
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 36483657
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 136154
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).
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 448454
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 225231
Psoni, L, Tzanetakis, N & Litopoulou-Tzanetaki, E 2003 Microbiological characteristics of Batzos, a traditional Greek cheese from raw goat's milk. Food Microbiology 20 575582
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 676682
Sheehan, JJ 2007 What causes the development of gas during ripening? In Cheese Problems Solved, pp. 131132 (Ed. McSweeney, PLH). Abington: Woodhead Publishing Limited
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 123129
Tavaria, FK & Malcata, FX 1998 Microbiological characterization of Serra da Estrela cheese throughout its appellation d'Origine Protégée region. Journal of Food Protection 61 601607
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 240246
Tornadijo, ME, García, MC, Fresno, JM & Carballo, J 2001 Study of Enterobacteriaceae during the manufacture and ripening of San Simón cheese. Food Microbiology 18 499509
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 721728
Verdier-Metz, I, Michel, V, Delbès, C & Montel, MC 2009 Do milking practices influence the bacterial diversity of raw milk? Food Microbiology 26 305310
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 1720


Related content

Powered by UNSILO

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

  • Rafael Tabla (a1), Antonia Gómez (a1), Alfredo Simancas (a2), José Emilio Rebollo (a2), Felipe Molina (a2) and Isidro Roa (a1)...


Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.