Use of autolytic starter systems to accelerate the ripening of Cheddar cheese
Abstract
The rapid release of intracellular enzymes due to autolysis of lactic acid bacteria in the cheese matrix post-manufacture is thought to play a role in the acceleration of cheese ripening. To investigate this hypothesis Cheddar cheese was manufactured using three related starter systems which varied with respect to their autolytic properties. Starter system A contained a blend of two Lactococcus lactis strains (223 and 227) which had a low level of autolysis. System B was identical to A but included an adjunct of a highly autolytic strain of Lactobacillus helveticus (DPC4571). System C consisted only of strain DPC4571 as starter. The cheeses were evaluated during ripening for key ripening indices including autolysis of starter cells by release of intracellular marker enzyme lactate dehydrogenase (LDH), composition, proteolysis and flavour development by descriptive sensory analysis. Populations of Lb. helveticus DPC4571 decreased rapidly in cheeses B and C and were not detected by 8 weeks. The level of starter culture autolysis proceeded in the order C≫B>A. Levels of proteolysis were elevated in cheeses B and C relative to A. Principal component analysis of the sensory data separated the character of cheese A from that of cheeses B and C. Cheeses B and C developed a unique ‘balanced’ ‘strong’ flavour early in ripening with a ‘caramel’ and ‘musty’ odour and ‘sweet’ ‘astringent’ flavour compared to cheese A. Hierarchical cluster analysis grouped C at 2 months with B at 6 and 8 months reflecting accelerated flavour development. Proteolytic and sensory data support the hypothesis that autolysis accelerates the rate of cheese ripening.
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The SN% results are in agreement with studies by Hannon et al. (2003), Jahadi and Khosravi-Darani (2017), Kaminaries et al. (2019), and Nuñez et al. (1991).
“Moreover, it resulted is in agreement with the study of other scientists such as Hannon et al. (2003); Jahadi and Khosravi-Darani (2017); Kaminaries et al. (2019); Nuñez et al. (1991).”
From Optimizing the acceleration of Cheddar cheese ripening using response surface methodology by microbial protease without altering its quality features (2021) · cites this paper as Hannon et al. (2003)
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“helveticus strains as adjunct cultures for the manufacture of Cheddar cheese ripened for 8 mo (Hanon et al., 2003) and Swiss cheese ripened for 3 mo (Valence et al.”
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“Similarly, it was reported that further hydrolysis of peptides by Lb. helveticus in Cheddar cheese during ripening was reported (Hannon et al. 2003).”
BackgroundDetection and enumeration of Lactobacillus helveticus in dairy products
Moser, A. I., Berthoud, H., Eugster, E., Meile, L., & Irmler, S. (2016) · International Dairy Journal · doi:10.1016/j.idairyj.2016.12.007 · Cited by 38 · see citing works
Hickey, C. D., Fallico, V., Wilkinson, M. G., & Sheehan, J. J. (2017) · Food Microbiology · doi:10.1016/j.fm.2017.08.015 · Cited by 38 · see citing works
Self-citationThe relative contributions of starter cultures and non-starter bacteria to the flavour of cheese
Gobbetti, M., Angelis, M. D., Cagno, R. D., & Rizzello, C. G. (2007) · Elsevier eBooks · doi:10.1533/9781845693053.1.121 · Cited by 38 · see citing works
Lysis of starters in UF cheeses: Behaviour of mesophilic lactococci and thermophilic lactobacilli
Hannon, J. A., Deutsch, S., Madec, M., Gassi, J.-Y., Chapot, M.-P., & Lortal, S. (2005) · International Dairy Journal · doi:10.1016/j.idairyj.2005.04.003 · Cited by 38 · see citing works
“The detection of cytoplasmic enzymes, lactate dehydrogenase (LDH), glucose-6phosphate dehydrogenase (G6PDH), X-prolyl-dipeptidyl-aminopeptidase (Pep-X) and lysyl-aminopeptidase have been used successfully as lysis markers (Crow et al., 1995; Hannon et al., 2003; Kiernan, Beresford, O’Cuinn, & Jordan, 2000; Wilkinson e…”
BackgroundMethodInfluentialSelf-citationHickey, C. D., Diehl, B. W. K., Nuzzo, M., Millqvist-Feurby, A., Wilkinson, M. G., & Sheehan, J. J. (2017) · Food Research International · doi:10.1016/j.foodres.2017.09.067 · Cited by 37 · see citing works
“However, lactococcal LDH requires a co-factor, fructose-1,6 bis-phosphate (FBP), for activation (Hannon et al. 2003, Yarlagadda et al. 2014).”
BackgroundResultInfluentialSelf-citationKaraca, O. B., & Güven, M. (2018) · Foods · doi:10.3390/foods7080125 · Cited by 37 · see citing works
“Water soluble nitrogen (WSN) ratio [30], 5% phosphotungstic acid soluble nitrogen (PTA-SN) ratio [31] and 12% trichloroacetic acid soluble nitrogen ratio (TCA-SN) [32] were determined with the Micro–Kjeldahl method [26].”
BackgroundInfluentialHou, J., Hannon, J. A., McSweeney, P. L. H., Beresford, T. P., & Guinee, T. P. (2012) · International Dairy Journal · doi:10.1016/j.idairyj.2011.12.015 · Cited by 33 · see citing works
Self-citationYarlagadda, A. B., Wilkinson, M. G., O’Sullivan, M. G., & Kilcawley, K. N. (2014) · International Dairy Journal · doi:10.1016/j.idairyj.2014.01.007 · Cited by 34 · see citing works
“helveticus strains (Hannon et al., 2003; Kenny, FitzGerald, O’Cuinn, Beresford, & Jordan, 2006; Kiernan, Beresford, O’Cuinn, & Jordan, 2000).”
BackgroundResultInfluentialSelf-citationCharacterisation of biochemical changes during ripening in Argentinean sheep cheeses
Bergamini, C. V., Wolf, I. V., Perotti, M. C., & Zalazar, C. A. (2010) · Small Ruminant Research · doi:10.1016/j.smallrumres.2010.07.004 · Cited by 33 · see citing works
Doolan, I. A., & Wilkinson, M. (2009) · International Dairy Journal · doi:10.1016/j.idairyj.2008.11.003 · Cited by 33 · see citing works
“lactis HP release lower levels of intracellular enzymes into cheese and may produce a bitter tasting cheese (Boutrou et al., 1998; Hannon et al., 2003; Lowrie et al., 1972; Martley and Lawrence, 1972; O’Donovan et al., 1996; Pillidge et al., 2002; Sheehan et al., 2006; Wilkinson et al., 1994, 1995).”
BackgroundSelf-citationRipening of extra-hard cheese made with mesophilic DL-starter
Rehn, U., Petersen, M. A., Saedén, K. H., & Ardö, Y. (2010) · International Dairy Journal · doi:10.1016/j.idairyj.2010.06.001 · Cited by 32 · see citing works
Hannon, J. A., Lopez, C., Madec, M., & Lortal, S. (2006) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(06)72144-0 · Cited by 32 · see citing works
“and improved organoleptic properties in traditional types of cheese have been well documented (ChapotChartier et al., 1994; Wilkinson et al., 1994; Deutsch et al., 2002; Hannon et al., 2003; Lortal and ChapotChartier, 2005).”
BackgroundSelf-citationOluk, C. A., Güven, M., & Hayaloğlu, A. A. (2013) · International Journal of Food Science & Technology · doi:10.1111/ijfs.12320 · Cited by 31 · see citing works
Møller, K. K., Rattray, F. P., Høier, E., & Ardö, Y. (2012) · Dairy Science and Technology · doi:10.1007/s13594-012-0090-5 · Cited by 30 · see citing works
“The approach of introducing a controlled level of lysis represents one means of increasing the ratio of peptidase to proteinase activity in the cheese and has demonstrated a potential to accelerate ripening and counteract bitterness development (Hannon et al. 2003; Lowrie et al. 1972).”
BackgroundHerreros, M. A., Arenas, R. L. S., Sandoval, M. H. L., Castro, J. M., Fresno, J. M., & Tornadijo, M. E. (2006) · International Dairy Journal · doi:10.1016/j.idairyj.2006.04.005 · Cited by 29 · see citing works
Technological characteristics of Lactobacillus spp. isolated from Iranian raw milk Motal cheese
Nezhad, S. J. E., Dovom, M. R. E., Najafi, M. B. H., Yavarmanesh, M., & Mayo, B. (2020) · LWT · doi:10.1016/j.lwt.2020.110070 · Cited by 29 · see citing works
Vázquez-Velázquez, R., Salvador-Figueroa, M., Adriano-Anaya, L., DeGyves–Córdova, G., & Vázquez-Ovando, A. (2018) · CyTA - Journal of Food · doi:10.1080/19476337.2017.1420694 · Cited by 29 · see citing works
“…of precursors (Hannon, Kilcawley, Wilkinson, Delahunty, & Beresford, 2007); or c) the Lactobacillus which make up these treatments do not permit the development of other LAB (nonstarters) which it is argued in some matured cheeses are responsible for the ultimate flavor (Hannon et al., 2003).”
BackgroundAyağ, N., Daǧdemi̇r, E., & Hayaloğlu, A. A. (2021) · International Dairy Journal · doi:10.1016/j.idairyj.2021.105285 · Cited by 27 · see citing works
Starter Bacteria Are the Prime Agents of Lipolysis in Cheddar Cheese
Hickey, D. K., Kilcawley, K. N., Beresford, T. P. J., & Wilkinson, M. G. (2006) · Journal of Agricultural and Food Chemistry · doi:10.1021/jf060819h · Cited by 27 · see citing works
Self-citationDorau, R., Chen, J., Liu, J., Jensen, P. R., & Solem, C. (2021) · Applied and Environmental Microbiology · doi:10.1128/aem.01035-21 · Cited by 29 · see citing works
“cremoris, which autolyze well under the processing conditions (10, 22, 24, 25).”
BackgroundAcceleration of cheese ripening
Upadhyay, V. K., & McSweeney, P. L. H. (2003) · Elsevier eBooks · doi:10.1533/9781855737075.3.419 · Cited by 26 · see citing works
Upadhyay, V. K., Huppertz, T., Kelly, A. L., & McSweeney, P. L. H. (2007) · Innovative Food Science & Emerging Technologies · doi:10.1016/j.ifset.2007.04.013 · Cited by 26 · see citing works
Treimo, J., Vegarud, G. E., Langsrud, T., & Rudi, K. (2006) · Applied and Environmental Microbiology · doi:10.1128/aem.00515-06 · Cited by 24 · see citing works
“a Different isomers of LDH (10) or requirements for a cofactor for LDH activation (14) make differentiation achievable.”
BackgroundGarde, S., Ávila, M., Fernández-Garcı́a, E., Médina, M., & Núñez, M. (2006) · International Dairy Journal · doi:10.1016/j.idairyj.2006.07.005 · Cited by 23 · see citing works
“helveticus strains and accelerated flavour development has been shown for Cheddar (Hanon et al., 2003; Kiernan, Beresford, O’Cuinn, & Jordan, 2000) and Swiss (Valence, Deutsch, Richoux, Gagnaire, & Lortal, 2000) cheeses.”
BackgroundAlhelli, A. M., Mohammed, N. K., Khalil, E. S., & Hussin, A. S. M. (2021) · AMB Express · doi:10.1186/s13568-021-01205-9 · Cited by 23 · see citing works
Callanan, M. J., Beresford, T. P. J., & Ross, R. P. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.3.1655-1658.2005 · Cited by 22 · see citing works
“The strain demonstrates a number of highly desirable traits including rapid autolysis, reduced bitterness, and increased flavor notes in cheese (6, 7).”
BackgroundSelf-citationTarakçı, Z., & Deveci, F. (2019) · Mljekarstvo/Mljekarstvo.com · doi:10.15567/mljekarstvo.2019.0106 · Cited by 22 · see citing works
“CC 3.40±0.41 4.01±0.23 4.94±0.02 5.40±0.12 7.88±0.16 5.13±1.56ab B1 3.15±0.15 3.94±0.08 4.87±0.01 4.97±0.05 9.12±0.27 5.21±2.07b B2 3.26±0.01 4.33±0.24 5.57±0.28 6.13±0.15 10.73±0.10 6.00±2.57c B3 3.64±0.32 4.07±0.29 6.75±0.03 7.12±0.11 11.05±0.35 6.53±2.67d B4 3.83±0.06 4.15±0.20 6.05±0.43 5.51±0.06 7.35±0.14 5.38±1.…”
BackgroundInfluentialÁvila, M., Garde, S., Médina, M., & Núñez, M. (2005) · Journal of Food Protection · doi:10.4315/0362-028x-68.5.1026 · Cited by 21 · see citing works
Søndergaard, L., Ryssel, M., Svendsen, C., Høier, E., Andersen, U., Hammershøj, M., Møller, J. R., Arneborg, N., & Jespersen, L. (2015) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2015.06.031 · Cited by 20 · see citing works
Doolan, I. A., Nongonierma, A. B., Kilcawley, K. N., & Wilkinson, M. G. (2013) · International Dairy Journal · doi:10.1016/j.idairyj.2013.07.005 · Cited by 19 · see citing works
“Acceleration of ripening time and/or flavour modification in Cheddar cheese has been undertaken in a number of studies involving addition of exogenous proteolytic preparations either with cheesemilk or at the salting stage (El Soda & Pandian, 1991; Hannon et al., 2003; Kailasapathy & Lam, 2005; Madkor, Tong, & El Soda…”
BackgroundSelf-citationTerzic-Vidojevic, A., Mihajlovic, S., Uzelac, G., Golic, N., Fira, D., Kojic, M., & Topisirovic, L. (2014) · Archives of Biological Sciences · doi:10.2298/abs1401179t · Cited by 18 · see citing works
“In addition, many LAB species play an important role in the ripening process of cheese, especially to improve the consistency, aroma and flavor (Giraffa, 2002; Hannon et al., 2003; Duan et al., 2008).”
BackgroundŞahingil, D., Gokce, Y., Yüceer, M., & Hayaloğlu, A. A. (2018) · LWT · doi:10.1016/j.lwt.2018.09.076 · Cited by 18 · see citing works
Spus, M., Liu, H., Wels, M., Abee, T., & Smid, E. J. (2016) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2016.10.020 · Cited by 18 · see citing works
“LDH is regarded as a good indicator of bacterial lysis (Hannon et al., 2003).”
BackgroundEsen, M. K., & Güzeler, N. (2022) · International Dairy Journal · doi:10.1016/j.idairyj.2022.105519 · Cited by 17 · see citing works
Machine learning for the prediction of proteolysis in Mozzarella and Cheddar cheese
Golzarijalal, M., Ong, L., Neoh, C. R., Harvie, D. J. E., & Gras, S. L. (2024) · Food and Bioproducts Processing · doi:10.1016/j.fbp.2024.01.009 · Cited by 18 · see citing works
Cheese manufacture and ripening and their influence on cheese flavour
McSweeney, P. L. H. (2007) · Elsevier eBooks · doi:10.1533/9781845693053.1 · Cited by 16 · see citing works
O'Brien, E., Mills, S., Dobson, A., Serrano, L., Hannon, J. A., Ryan, S. P., Kilcawley, K. N., Brandsma, J. B., Meijer, W. C., Hill, C., et al. (2017) · Journal of Dairy Science · doi:10.3168/jds.2016-11726 · Cited by 15 · see citing works
“This was presumably due to a combination of a nisin-producing operon and the autolytic nature of the DVI used, because these characteristics are commonly associated with a greater concentration of free amino acids (Chapot-Chartier et al., 1994; Wilkinson et al., 1994a,b; Benech et al., 2003; Hannon et al., 2003).”
BackgroundSelf-citationOneca, M., Ortigosa, M., Irigoyen, A., & Torre, P. (2006) · Food Chemistry · doi:10.1016/j.foodchem.2005.11.056 · Cited by 15 · see citing works
Growth, survival, and peptidolytic activity of Lactobacillus plantarum I91 in a hard-cheese model
Bergamini, C. V., Peralta, G. H., Milesi, M. M., & Hynes, E. R. (2013) · Journal of Dairy Science · doi:10.3168/jds.2013-6567 · Cited by 15 · see citing works
“…that autolytic starters were favorable for the growth of NSLAB because their cellular contents could provide the NSLAB with carbohydrates (Thomas, 1987), and their intracellular enzymes increased the pool of peptides and amino acids (Kiernan et al., 2000; Hannon et al., 2003; Kenny et al., 2006).”
BackgroundLee, B. H., Kilcawley, K. N., Hannon, J. A., Park, S. Y., Wilkinson, M. G., & Beresford, T. P. J. (2007) · Food Biotechnology · doi:10.1080/08905430701410530 · Cited by 15 · see citing works
“helveticus have very high levels of peptidases ( Khalid and Marth, 1990 ; Park et al, 1995 ; Hannon et al, 2003 ), which would be released in lysed cells.”
BackgroundSelf-citationSuja Rani, S., Prajapati, J. B., & Joshi, C. G. (2014) · Genome · doi:10.1139/gen-2014-0020 · Cited by 14 · see citing works
“Lactobacillus helveticus DPC 4571, a Swiss cheese isolate, is used as a starter and adjunct culture for rapid autolysis, reduced bitterness, and increased flavor notes in cheese (Hannon et al. 2003).”
BackgroundEffect of growth phase and growth medium on peptidase activities of starter lactic acid bacteria
Simova, E. D., & Бешкова, Д. (2007) · Le Lait · doi:10.1051/lait:2007036 · Cited by 13 · see citing works
“In recent years, researchers have recognized the importance of the proteolytic system of lactobacilli for cheese ripening and cheese quality [9, 10, 18, 22].”
BackgroundCheese Microbial Ecology and Safety
Picón, A. (2017) · Wiley eBooks · doi:10.1002/9781119046165.ch0d · Cited by 13 · see citing works
Garbowska, M., Pluta, A., & Berthold-Pluta, A. (2016) · LWT - Food Science and Technology · doi:10.1016/j.lwt.2016.01.044 · Cited by 12 · see citing works
Gürmeriç, H. E., Şengül, M., & Erkaya, T. (2024) · Food Bioscience · doi:10.1016/j.fbio.2024.103812 · Cited by 12 · see citing works
Jebavá, I., Plocková, M., Lortal, S., & Valence, F. (2011) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2011.04.015 · Cited by 12 · see citing works
Peralta, G. H., Bergamini, C. V., & Hynes, E. R. (2019) · International Dairy Journal · doi:10.1016/j.idairyj.2019.01.002 · Cited by 11 · see citing works
Candioti, M. C., Bergamini, C. V., Palma, S. B., Busetti, M. R., Meinardi, C. A., & Zalazar, C. A. (2009) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.3776 · Cited by 10 · see citing works
Proteolysis in the Beyaz (White) Cheese Produced From Various Milk
Öner, Z., & Sarıdağ, M. (2018) · Tarım Bilimleri Dergisi · doi:10.15832/ankutbd.446454 · Cited by 10 · see citing works
“It was reported that the fractions of nitrogen soluble in 5% PTA in the cheese included peptides smaller than 600-700 Dalton (di-, tri-and tetra-peptides) and amino acids (Mc Sweeney & Fox 1997; Hannon et al 2003).”
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Ertekin, M., Uğurlu, Ö., Salum, P., & Erbay, Z. (2023) · Journal of Food Science · doi:10.1111/1750-3841.16519 · Cited by 9 · see citing works
The effects of different salting and preservation techniques ofkaşar cheese on cheese quality
Çeti̇nkaya, A., & Atasever, M. (2015) · TURKISH JOURNAL OF VETERINARY AND ANIMAL SCIENCES · doi:10.3906/vet-1407-74 · Cited by 9 · see citing works
“Salt content (%) was determined with the Mohr method (7), and the pH value with a pH meter (WTW3510i) (9).”
MethodSoft white cheese ripening using bacterial protease enzyme
El-Salam, B. A. E.-Y. A., Ahmed, M. S., Yasser, M. M., & Taha, S. S. E.-D. (2019) · Acta Scientiarum Polonorum Technologia Alimentaria · doi:10.17306/j.afs.0665 · Cited by 9 · see citing works
“Studies on pickled cheeses have reported that the pH value of cheeses changed depending on the ripening duration and temperature (Hannon et al., 2003; Hayaloglu, 2003).”
BackgroundÇeti̇nkaya, A. (2021) · GIDA / THE JOURNAL OF FOOD · doi:10.15237/gida.gd21060 · Cited by 9 · see citing works
Insertion sequence elements as mediators of strain diversity in Lactobacillus helveticus
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Self-citationIn vivo Evaluation of Safety and Probiotic Traits of Isolated Enterococcus feacium Strain KT712
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Cheng, T., Lin, W. A. N. G., Guo, Z., & Li, B. (2022) · Food Science and Technology · doi:10.1590/fst.13022 · Cited by 10 · see citing works
Technological characterisation of Lactobacilli isolated from Chinese artisanal fermented milks
Ma, C., Zhang, L., Ma, D., Du, M., Han, X., Yi, H., Zhang, L., Feng, Z. G., Zhang, Y., Zhang, Y., et al. (2011) · International Journal of Dairy Technology · doi:10.1111/j.1471-0307.2011.00743.x · Cited by 8 · see citing works
Bitterness masking effects of carob syrup in bitter orange (Citrus aurantium) jam production
Özbek, Ç. (2023) · Journal of Food Measurement & Characterization · doi:10.1007/s11694-023-01989-3 · Cited by 7 · see citing works
Yilmaz, F., Daǧdemi̇r, E., & Hayaloğlu, A. A. (2025) · Food Chemistry · doi:10.1016/j.foodchem.2025.144090 · Cited by 7 · see citing works
- Authors
- Hannon, J. A., Wilkinson, M. G., Delahunty, C. M., Wallace, J. M., Morrissey, P. A., & Beresford, T. P.
- Affiliations
- Teagasc - The Irish Agriculture and Food Development Authority (IE)
- University of Limerick (IE)
- University College Cork (IE)
- Corresponding author
- Beresford, T.P.
- Venue
- International Dairy Journal
- Publisher
- Elsevier BV
- Published
- 2003-01
- Volume
- 13
- Issue
- 4
- Pages
- 313-323
- ISSN
- 0958-6946 (ISSN-L)
- OpenAlex
- W1964764457
- Cited by
- 141
- References
- 51
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 4 · 2023: 9 · 2022: 4 · 2021: 11 · 2020: 3 · 2019: 4 · 2018: 5 · 2017: 8 · 2016: 7 · 2015: 4 · 2014: 7 · 2013: 10 · 2012: 3
- FWCI
- 14.14
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- International Dairy Journal (publishedVersion)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Life Sciences › Agricultural and Biological Sciences › Food Science › Fermentation and Sensory Analysis
- Life Sciences › Agricultural and Biological Sciences › Food Science › Advanced Scientific Research Methods
- Keywords
- Cheddar cheese, cheese ripening, starter cultures, autolysis, Lactobacillus helveticus, Lactococcus lactis, intracellular enzymes, lactate dehydrogenase, proteolysis, flavour development, cheese composition, starter culture viability
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