Studying enterococci isolated from artisanal feta produced with mountain and low land milk


E Psomas
I Sakaridis
E Boukouvala
E Papatsaroucha
ED Apostolidi
T Skarlatoudi
LV Ekateriniadou
Georgios Samouris
Résumé

Enterococci are commonly part of natural milk cultures that are used to produce cheese and have a strong influence on ripening, and aroma development in feta cheese. Despite their unique benefits in cheese production, Enterococci have also been identified as opportunistic pathogens that can cause various human diseases and their use remains controversial due to the possibility of antimicrobial resistance transfer to human strains. The objective of the present study was to detect, identify, and analyze characteristics of Enterococcus spp. from different samples of the artisanal feta cheese produced with mountain or low land milk and finally to evaluate its potential use for enhancing the sensory characteristics of fermented milks and cheeses without compromising the safety of the products. Twenty-five strains of enterococci from mountain areas and twenty-five from low land areas were selected from the cheesemaking trials. Based on the desired technological characteristics, twelve strains were selected for analytical identification, study of antibiotic resistance and further study by molecular techniques. Eleven of those were found to be sensitive to vancomycin (lower to 10μg/ml), one was resistant up to 20μg/ml and therefore are even more promising, in terms of their safety, for their potential use as adjunct cultures and worth further analysis.

Article Details
  • Rubrique
  • Research Articles
Téléchargements
Les données relatives au téléchargement ne sont pas encore disponibles.
Références
Anifantakis EM (1991) In: Greek Cheeses: A Tradition of Centuries; Na
tional Dairy Committee of Greece, Athens, Greece: pp. 49-69.
Alexandraki V, Kazou M, Angelopoulou A, Arena MP, Capozzi V, Russo
P, Fiocco D, Spano G,
Papadimitriou K, Tsakalidou E (2016) The Microbiota of Non-Cow
Milk and Products. In: Non-Bovine Milk and Milk Products, Aca
demic Press, Cambridge, Massachusetts, United States: pp. 117-159.
Aspri M, Bozoudi D, Tsaltas D, Hill C, Papademas P (2017) Raw Donkey
Milk as a Source of Enterococcus
Diversity: Assessment of
Their Technological Properties and Safety Characteristics. Food Con
trol 73:81-90.
Bastião Rocha PA, Monteiro Marques JM, Barreto AS, Semedo-Lemsad
dek T (2022) Enterococcus Spp.
from Azeitão and Nisa
PDO-Cheeses: Surveillance for Antimicrobial Drug Resistance.
LWT 154:112622.
Bonham KS, Wolfe BE, Dutton RJ (2017) Extensive Horizontal Gene
Transfer in Cheese-Associated
Food Microbiol 88:215-222.
Gomes BC, Esteves CT, Palazzo ICV, Darini ALC, Felis GE, Sechi
LA, Franco BDGM, de Martinis
ECP (2008) Prevalence
and Characterization of Enterococcus Spp. Isolated from Brazilian
Foods.
Food Microbiol 25:668-675.
Graham K, Stack H, Rea R (2020) Safety, Beneficial and Technological
Properties of Enterococci for Use in
Functional Food Applica
tions - a Review. Crit Rev Food Sci Nutr 60:3836-3861.
Harrigan WF, McCance ME (1976) In: Laboratory Methods in Food and
Dairy Microbiology, Rev.ed, Academic Press Inc. Limited, London,
UK: pp. 226-227.
İspirli H, Demirbaş F, Dertli E (2017) Characterization of Functional
Properties of Enterococcus Spp.
Isolated from Turkish White
Cheese. LWT 75:358-365.
Jurkovič D, Križková L, Dušinský R, Belicová A, Sojka M, Krajčovič J,
Ebringer L (2006) Identification
Bacteria. Elife 6:e22144.
Centeno JA, Menéndez S, Rodríguez-Otero JL (1996) Main Microbial
Flora Present as Natural Starters in
Cebreiro Raw Cow’s-Milk
Cheese (Northwest Spain). Int J Food Microbiol 33:307-313.
CLSI Supplement M100 (2020), In: CLSI. Performance Standards for
Antimicrobial Susceptibility Testing.
th ed, Wayne, PA: Clini
cal and Laboratory Standards Institute.
Durlu-Ozkaya F, Xanthopoulos V, Tunail N, Litopoulou-Tzanetaki E
(2001) Technologically Important
Properties of Lactic Acid
Bacteria Isolates from Beyaz Cheese Made from Raw Ewes’ Milk. J
Appl Microbiol 91:861-870.
EFSA Panel on Additives and Products or Substances used in Animal
Feed (FEEDAP), Rychen G, Aquilina G, Azimonti G, Bampidis V,
Bastos M de L, Bories G, Chesson A, Cocconcelli PS, Flachowsky
G,
Gropp J, Kolar B, Kouba M, López-Alonso M, López Puente
S, Mantovani A, Mayo B, Ramos
F,
Saarela M, Villa
RE, Wallace RJ, Wester P, Glandorf B, Herman L, Kärenlampi S,
Aguilera J,
Anguita M, Brozzi R, Galobart J (2018) Guidance
on the Characterisation of Microorganisms Used
Feed Addi
tives or as Production Organisms. EFSA Journal 16(3):e5206.
as
EFSA Panel on Biological Hazards (BIOHAZ), Koutsoumanis K, Allende
A, Álvarez-Ordóñez A, Bolton D,
Bover-Cid S, Chemaly M,
Davies R, de Cesare A, Herman L, Hilbert F, Lindqvist R, Nauta M,
Ru G, Simmons M, Skandamis P, Suffredini E, Argüello H, Beren
donk T, Cavaco LM, Gaze W, Schmitt H,
Topp E, Guerra
B, Liébana E, Stella P, Peixe L (2021) Role Played by the Environ
ment in the
Emergence and Spread of Antimicrobial Resistance
(AMR) through the Food Chain. EFSA Journal 19:e06651.
Erginkaya Z, Turhan EU, Tatli D (2018) Determination of Antibiotic Re
sistance of Lactic Acid Bacteria
Isolated from Traditional
Turkish Fermented Dairy Products. Iran J Vet Res 19:53.
Floros G, Hatzikamari M, Litopoulou-Tzanetaki E, Tzanetakis N (2012)
Probiotic and Technological Properties of Facultatively Heterofer
mentative Lactobacilli from Greek Traditional Cheeses. Food B i o
technol 26:85-105.
Franz CMAP, Stiles ME, Schleifer KH, Holzapfel WH (2003) Enterococ
ci in Foods - A Conundrum for
Food Safety. Int J Food Mi
crobiol 88:105-122.
Fusco V, Quero GM, Poltronieri P, Morea M, Baruzzi F (2019) Autoch
thonous and Probiotic Lactic Acid
Bacteria Employed for Pro
duction of “Advanced Traditional Cheeses.” Foods 8(9):412.
Georgieva M, Andonova L, Peikova L, Zlatkov A (2014) Probiotics -
Health Benefits, Classification,
Quality
Assurance
and
Quality Control - Review. Pharmacia 61:22-31.
Giménez-Pereira ML (2005) Enterococci in Milk Products : A Disserta
tion Presented in Partial Fulfilment of the Requirements for the
Degree of Master of Veterinary Studies at Massey University, Palm
erston North, New Zealand.
Giraffa G (2003) Functionality of Enterococci in Dairy Products. Int J
and Characterization of En
terococci from Bryndza Cheese. Lett Appl Microbiol 42:553-559.
Lianou DT, Fthenakis GC (2022) Use of Antibiotics against Bacterial In
fections on Dairy Sheep and Goat
Farms: Patterns of Usage
and Associations with Health Management and Human Resources.
Antibiotics 11:753.
Litopoulou-Tzanetaki E, Tzanetakis N (2014) The Microfloras of Tradi
tional Greek Cheeses.
MicrobiolSpectr 2: CM-0009-2012.
Manolopoulou E, Sarantinopoulos P, Zoidou E, Aktypis A, Moschopoulou
E, Kandarakis IG, Anifantakis
EM (2003) Evolution of Mi
crobial Populations during Traditional Feta Cheese Manufacture and
Ripening. Int J Food Microbiol 82:153-161.
Ogier JC, Serror P (2008) Safety Assessment of Dairy Microorganisms:
The Enterococcus Genus. Int J Food
Microbiol 126:291-301.
Psomas E, Sakaridis I, Boukouvala E, Karatzia MA, Ekateriniadou LV,
Samouris G (2023) Indigenous
Lactic Acid Bacteria Isolat
ed from Raw Graviera Cheese and Evaluation of Their Most Import
ant
Technological Properties. Foods 12:370.
Rantsiou K, Urso R, Dolci P, Comi G, Cocolin L (2008) Microflora of
Feta Cheese from Four Greek
Manufacturers. Int J Food
Microbiol 126:36-42.
Routray W, Mishra HN (2011) Scientific and Technical Aspects of Yogurt
Aroma and Taste: A Review. Compr Rev Food Sci Food Saf 10:208
Sarantinopoulos P, Andrighetto C, Georgalaki MD, Rea MC, Lombardi A,
Cogan TM, Kalantzopoulos G,
Tsakalidou E (2001) Bio
chemical Properties of Enterococci Relevant to Their Technological
Performance. Int Dairy J 11:621-647.
Sarantinopoulos P, Kalantzopoulos G, Tsakalidou E (2000a) Effect of En
terococcus Faecium on
Microbiological, Physicochemical and
Sensory Characteristics of Greek Feta Cheese. Int J Food
M i
crobiol 76:93-105.
Sarantinopoulos P, Leroy F, Leontopoulou E, Georgalaki MD, Kalantzo
poulos G, Tsakalidou E, De VL
(2002b) Bacteriocin Produc
tion by Enterococcus Faecium FAIR-E 198 in View of Its Application
as
Adjunct Starter in Greek Feta Cheese Making. Int J Food Mi
crobiol 72(1-2):125-136.
Schillinger U, Lücke FK (1987) Identification of Lactobacilli from Meat
and Meat Products. Food Microbiol
:199-208.
Settanni L, Moschetti G (2012) Non-Starter Lactic Acid Bacteria Used to
Improve Cheese Quality and
Provide Health Benefits.
Food Microbiol 27:691-697.
Suzzi G, Caruso M, Gardini F, Lombardi A, Vannini L, Guerzoni ME,
Andrighetto C, Lanorte MT (2000) A Survey of the Enterococci
Isolated from an Artisanal Italian Goat’s Cheese (SemicottoCaprino).
J
Appl Microbiol 89:267-274.
Terzić-Vidojević A, Veljović K, Popović N, Tolinački M, Golić N (2021)
Enterococci from Raw-Milk Cheeses: Current Knowledge on Safety,
Technological, and Probiotic Concerns. Foods 10:2753.
Tsakalidou ME, Tsilibari V, Georgalaki M, Kalantzopoulos G (1993) Es terolytic Activities of Enterococcus
Durans and Enterococcus
Faecium Strains Isolated from Greek Cheese. Netherland Milk Dairy
Journal 47:145-150.
Vanden Eng J, Marcus R, Hadler JL, Imhoff B, Vugia DJ, Cieslak PR, Zell
E, Deneen V, McCombs KG,
Zansky
SM,
Hawkins
MA, Besser RE (2003) Consumer Attitudes and Use of Antibiotics.
Emerg
Infect Dis 9:1128-1135.
Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, Schleifer
KH, Whitman WB (2009) The
Firmicutes. In: Bergey’s
manual of systematic bacteriology, Vol. 3, Springer-Verlag, New
York, United States: pp. 1145-1145.
Výrostková J, Regecová I, Dudriková E, Marcinčák S, Vargová M,
Kováčová M, Mal’ová J (2021)
Antimicrobial Resistance of
Enterococcus sp. Isolated from Sheep and Goat Cheeses. Foods
(8):1844.
Yerlikaya O, Akbulut N (2020) In Vitro Characterisation of Probiotic
Properties of Enterococcus Faecium
and Enterococcus Durans
Strains Isolated from Raw Milk and Traditional Dairy Products. Int J
Dairy Technol 73:98-107.