Microbial Profile Antibacterial Properties and Chemical Composition of Raw Donkey Milk
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Animals and Sampling
2.2. Chemical Analyses
2.3. Microbiological and Somatic Cell Count Analyses
2.4. Bacterial Isolation and Identification
2.5. Antimicrobial Activity Assay
2.6. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Guo, H.Y.; Pang, K.; Zhang, X.Y.; Zhao, L.; Chen, S.W.; Dong, M.L.; Ren, F.Z. Composition, physiochemical properties, nitrogen fraction distribution, and amino acid profile of donkey milk. J. Dairy Sci. 2007, 90, 1635–1643. [Google Scholar] [CrossRef] [PubMed]
- Claeys, W.; Verraes, C.; Cardoen, S.; De Block, J.; Huyghebaert, A.; Raes, K.; Dewettinck, K.; Herman, L. Consumption of raw or heated milk from different species: An evaluation of the nutritional and potential health benefits. Food Control 2014, 42, 188–201. [Google Scholar] [CrossRef]
- Gastaldi, D.; Bertino, E.; Monti, G.; Baro, C.; Fabris, C.; Lezo, A.; Medana, C.; Baiocchi, C.; Mussap, M.; Galvano, F. Donkey’s milk detailed lipid composition. Front. Biosci. 2010, 2, 537–546. [Google Scholar]
- Martemucci, G.; D’Alessandro, A.G. Fat content, energy value and fatty acid profile of donkey milk during lactation and implications for human nutrition. Lipids Health Dis. 2012, 11, 113. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martini, M.; Altomonte, I.; Salari, F.; Caroli, A.M. Short communication: Monitoring nutritional quality of Amiata donkey milk: Effects of lactation and productive season. J. Dairy Sci. 2014, 97, 6819–6822. [Google Scholar] [CrossRef]
- Salimei, E.; Fantuz, F. Equid milk for human consumption. Int. Dairy J. 2012, 24, 130–142. [Google Scholar] [CrossRef]
- Tafaro, A.; Magrone, T.; Jirillo, F.; Martemucci, G.; D’Alessandro, A.G.; Amati, L.; Jirillo, E. Immunological properties of donkey’s milk: Its potential use in the prevention of atherosclerosis. Curr. Pharm. Des. 2007, 13, 3711–3717. [Google Scholar] [CrossRef]
- Mao, X.; Gu, J.; Sun, Y.; Xu, S.; Zhang, X.; Yang, H.; Ren, F. Anti-proliferative and anti-tumour effect of active components in donkey milk on A549 human lung cancer cells. Int. Dairy J. 2009, 19, 703–708. [Google Scholar] [CrossRef]
- Coppola, R.; Salimei, E.; Succi, M.; Sorrentino, E.; Nanni, M.; Ranieri, P.; Belliblanes, R.; Grazia, L. Behavior of Lactobacillus rhamnosus strains in ass’s milk. Ann. Microbiol. 2002, 52, 55–60. [Google Scholar]
- Salimei, E.; Fantuz, F.; Coppola, R.; Chiofalo, B.; Polidori, P.; Varisco, G. Composition and characteristics of ass’s milk. Anim. Res. 2004, 53, 67–78. [Google Scholar] [CrossRef] [Green Version]
- Sarno, E.; Santoro, M.L.A.; Di Palo, R.; Costanzo, N. Microbiological quality of raw donkey milk from Campania Region. It. J. Anim. Sci. 2012, 11, e49. [Google Scholar] [CrossRef] [Green Version]
- Cavallarin, L.; Giribaldi, M.; de los Dolores Soto-Del, M.; Valle, E.; Barbarino, G.; Gennero, M.S.; Civera, T. A survey on the milk chemical and microbiological quality in dairy donkey farms located in North Western Italy. Food Control 2015, 50, 230–235. [Google Scholar] [CrossRef]
- Aspri, M.; Economou, N.; Papademas, P. Donkey milk: An overview on functionality, technology, and future prospects. Food Rev. Int. 2017, 33, 316–333. [Google Scholar] [CrossRef]
- Brumini, D.; Criscione, A.; Bordonaro, S.; Vegarud, G.E.; Marletta, D. Whey proteins and their antimicrobial properties in donkey milk: A brief review. Dairy Sci. Technol. 2016, 96, 1–14. [Google Scholar] [CrossRef] [Green Version]
- Bonomo, M.G.; Ricciardi, A.; Zotta, T.; Parente, E.; Salzano, G. Molecular and technological characterization of lactic acid bacteria from traditional fermented sausages of Basilicata region (Southern Italy). Meat Sci. 2008, 80, 1238–1248. [Google Scholar] [CrossRef]
- Paramithiotis, S.; Kouretas, K.; Drosinos, E.H. Effect of ripening stage on the development of the microbial community during spontaneous fermentation of green tomatoes. J. Sci. Food Agric. 2014, 94, 1600–1606. [Google Scholar] [CrossRef]
- Rantsiou, K.; Drosinos, E.H.; Gialitaki, M.; Metaxopoulos, I.; Comi, G.; Cocolin, L. Use of molecular tools to characterize Lactobacillus spp. isolated from Greek traditional fermented sausages. Int. J. Food Microbiol. 2006, 112, 215–222. [Google Scholar] [CrossRef]
- Sesena, S.; Sanchez, I.; Palop, L. Characterization of Lactobacillus strains and monitoring by RAPD-PCR in controlled fermentations of “Almagro” eggplants. Int. J. Food Microbiol. 2005, 104, 325–335. [Google Scholar] [CrossRef]
- ISO-IDF. ISO 9622: Milk and Liquid Milk Products–Guidelines for the Application of Mid-Infrared Spectrometry; IDF bulletin no. 141; International Organization for Standardization: Geneva, Switzerland; International Dairy Federation: Brussels, Belgium, 2013. [Google Scholar]
- Summer, A.; Sabbioni, A.; Formaggioni, P.; Mariani, P. Trend in ash and mineral element content of milk from Haflinger nursing mares throughout six lactation months. Livest. Prod. Sci. 2004, 88, 55–62. [Google Scholar] [CrossRef]
- ISO. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for the Enumeration of Mesophilic Lactic Acid Bacteria—Colony-Count Technique at 30 Degrees C; International Organization for Standardization: Geneva, Switzerland, 1998; ISO Standard 15214. [Google Scholar]
- International Dairy Federation (IDF). Milk and Milk Products—Count of Coliform Bacteria; IDF Reference Method 73; IDF: Brussels, Belgium, 1974. [Google Scholar]
- International Dairy Federation (IDF). Milk and Milk Products. Enumeration of Yeasts and Moulds. Colony Count Technique at 25 °C; IDF Standard 94B; IDF: Brussels, Belgium, 1990. [Google Scholar]
- ISO. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for the Enumeration of Presumptive Bacillus Cereus—Colony-Count Technique at 30 Degrees C; International Organization for Standardization: Geneva, Switzerland, 2004; ISO standard 7932. [Google Scholar]
- ISO. Milk-Enumeration of somatic cells—Part 2: Guidance on the operation of fluoro-opto-electronic counters. In IDF 148-2: 2006; ISO: Geneva, Switzerland, 2006; ISO standard 13366-2. [Google Scholar]
- Harrigan, W.F.; McCance, M.E. Laboratory Methods in Food and Dairy Microbiology; Academic Press: London, UK, 1976. [Google Scholar]
- Drosinos, E.H.; Paramithiotis, S.; Kolovos, G.; Tsikouras, I.; Metaxopoulos, I. Phenotypic and technological diversity of lactic acid bacteria and staphylococci isolated from traditionally fermented sausages in southern Greece. Food Microbiol. 2007, 24, 260–270. [Google Scholar] [CrossRef]
- Paramithiotis, S.; Tsiasiotou, S.; Drosinos, E.H. Comparative study of spontaneously fermented sourdoughs originating from two regions of Greece; Peloponnesus and Thessaly. Eur. Food Res. Technol. 2010, 231, 883–890. [Google Scholar] [CrossRef]
- Cocolin, L.; Rantsiou, K.; Iacumin, L.; Urso, R.; Cantoni, C.; Comi, G. Study of the ecology of fresh sausages and characterization of populations of lactic acid bacteria by molecular methods. Appl. Environ. Microbiol. 2004, 70, 1883–1894. [Google Scholar] [CrossRef] [Green Version]
- Hadjilouka, A.; Andritsos, N.D.; Paramithiotis, S.; Mataragas, M.; Drosinos, E.H. Listeria monocytogenes serotype prevalence and biodiversity in diverse food products. J. Food Prot. 2014, 77, 2115–2120. [Google Scholar] [CrossRef] [PubMed]
- Paramithiotis, S.; Kagkli, D.M.; Blana, V.A.; Nychas, G.J.; Drosinos, E.H. Identification and characterization of Enterococcus spp. in Greek spontaneous sausage fermentation. J. Food Prot. 2008, 71, 1244–1247. [Google Scholar] [CrossRef]
- Massouras, T.; Triantaphyllopoulos, K.A.; Theodossiou, I. Chemical composition, protein fraction and fatty acid profile of donkey milk during lactation. Int. Dairy J. 2017, 75, 83–90. [Google Scholar] [CrossRef]
- Malissiova, E.; Arsenos, G.; Papademas, P.; Fletouris, D.; Manouras, A.; Aspri, M.; Nikolopoulou, A.; Giannopoulou, A.; Arvanitoyannis, I.S. Assessment of donkey milk chemical, microbiological and sensory attributes in Greece and Cyprus. Int. J. Dairy Technol. 2016, 69, 143–146. [Google Scholar] [CrossRef]
- Ivanković, A.; Ramljak, J.; Štulina, I.; Antunac, N.; Bašić, I.; Kelava, N.; Konjačić, M. Characteristics of the lactation, chemical composition milk hygiene quality of the Littoral-Dinaric ass. Mljekarstvo 2009, 59, 107–113. [Google Scholar]
- Nazzaro, F.; Orlando, P.; Fratianni, F.; Coppola, R. Isolation of components with antimicrobial property from the donkey milk: A preliminary study. Open Food Sci. J. 2010, 4, 43–47. [Google Scholar] [CrossRef]
- Aspri, M.; Bozoudi, D.; Tsaltas, D.; Hill, C.; Papademas, P. Raw donkey milk as a source of Enterococcus diversity: Assessment of their technological properties and safety characteristics. Food Control 2017, 73, 81–90. [Google Scholar] [CrossRef]
- Conte, F.; Passantino, A. Guidelines for physical, chemical and hygienic quality and safety control of donkey’s milk. Milchwissenschaft 2009, 64, 85–88. [Google Scholar]
- Pilla, R.; Dapra, V.; Zecconi, A.; Piccinini, R. Hygienic and health characteristics of donkey milk during a follow-up study. J. Dairy Res. 2010, 77, 392–397. [Google Scholar] [CrossRef]
- Šarić, L.; Šarić, B.; Mandić, A.; Tomić, J.; Torbica, A.; Nedeljković, N.; Ikonić, B. Antibacterial activity of donkey milk against Salmonella. Agro Food Ind. Hi Tech 2014, 25, 30–34. [Google Scholar]
- Šarić, L.C.; Šarić, B.M.; Mandić, A.I.; Kevrešan, Z.S.; Ikonić, B.B.; Kravić, S.Z.; Jambrec, D.J. Role of calcium content in antibacterial activity of donkeys’ milk toward E. coli. Eur. Food Res. Technol. 2014, 239, 1031–1039. [Google Scholar] [CrossRef]
- Tidona, F.; Sekse, C.; Criscione, A.; Jacobsen, M.; Bordonaro, S.; Marletta, D.; Vegarud, G.E. Antimicrobial effect of donkeys’ milk digested in vitro with human gastrointestinal enzymes. Int. Dairy J. 2011, 21, 158–165. [Google Scholar] [CrossRef]
- Zhang, X.; Zhao, L.; Jiang, L.; Dong, M.; Ren, F. The antimicrobial activity of donkey milk and its microflora changes during storage. Food Control 2008, 19, 1191–1195. [Google Scholar] [CrossRef]
- Banwo, K.; Sanni, A.; Tan, H.; Tian, Y. Phenotypic and genotypic characterization of lactic acid bacteria isolated from some Nigerian traditional fermented foods. Food Biotechnol. 2012, 26, 124–142. [Google Scholar] [CrossRef]
- Fontana, C.; Sandro Cocconcelli, P.; Vignolo, G. Monitoring the bacterial population dynamics during fermentation of artisanal Argentinean sausages. Int. J. Food Microbiol. 2005, 103, 131–142. [Google Scholar] [CrossRef]
- Rossetti, L.; Giraffa, G. Rapid identification of dairy lactic acid bacteria by M13-generated, RAPD-PCR fingerprint databases. J. Microbiol. Meth. 2005, 63, 135–144. [Google Scholar] [CrossRef]
- Martin-Platero, A.M.; Maqueda, M.; Valdivia, E.; Purswani, J.; Martinez-Bueno, M. Polyphasic study of microbial communities of two Spanish farmhouse goats’ milk cheeses from Sierra de Aracena. Food Microbiol. 2009, 26, 294–304. [Google Scholar] [CrossRef]
- Tyler, K.D.; Wang, G.; Tyler, S.D.; Johnson, W.M. Factors affecting reliability and reproducibility of amplification-based DNA fingerprinting of representative bacterial pathogens. J. Clin. Microbiol. 1997, 35, 339–346. [Google Scholar] [CrossRef] [Green Version]
- Pulido, R.P.; Ben Omar, N.; Abriouel, H.; López, R.L.; Martınez Cañamero, M.; Gálvez, A. Microbiological study of lactic acid fermentation of caper berries by molecular and culture-dependent methods. Appl. Environ. Microbiol. 2005, 71, 7872–7879. [Google Scholar] [CrossRef] [Green Version]
- Feil, E.J.; Cooper, J.E.; Grundmann, H.; Robinson, D.A.; Enright, M.C.; Berendt, T.; Peacock, S.J.; Smith, J.M.; Murphy, M.; Spratt, B.G.; et al. How clonal is Staphylococcus aureus? J. Bacteriol. 2003, 185, 3307–3316. [Google Scholar] [CrossRef] [Green Version]
- Kelly, W.J.; Ward, L.J.; Leahy, S.C. Chromosomal diversity in Lactococcus lactis and the origin of dairy starter cultures. Genome Biol. Evol. 2010, 2, 729–744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carminati, D.; Tidona, F.; Fornasari, M.E.; Rossetti, L.; Meucci, A.; Giraffa, G. Biotyping of cultivable lactic acid bacteria isolated from donkey milk. Lett. Appl. Microbiol. 2014, 59, 299–305. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Breed | Animals/Lactation Period | Sampling Month | No. of Samples | ||||
---|---|---|---|---|---|---|---|
NOV | DEC | JAN | FEB | MAR | (n) | ||
Days | |||||||
C1 | 2 | 30 | 60 | 90 | 120 | 150 | 10 |
C2 | 4 | 60 | 90 | 120 | 150 | 180 | 20 |
C3 | 4 | 90 | 120 | 150 | 180 | 210 | 20 |
C4 | 2 | 120 | 150 | 180 | 210 | 240 | 10 |
C5 | 5 | 150 | 180 | 210 | 240 | 270 | 25 |
A1 | 6 | 30 | 60 | 90 | 120 | 150 | 30 |
Total | 23 | 115 |
C1 (n = 10) | C2 (n = 20) | C3 (n = 20) | C4 (n = 10) | C5 (n = 25) | A1 (n = 30) | p < 0.05 | |
---|---|---|---|---|---|---|---|
Fat (%) | 1.24 (0.6) | 0.85 (0.3) | 1.14 (0.3) | 1.20 (0.3) | 0.82 (0.1) | 1.05 (0.3) | ns |
Protein (%) | 1.36 (0.2) | 1.87 (0.2) | 1.30 (0.3) | 1.22 (0.2) | 1.27 (0.3) | 1.27 (0.1) | ns |
Lactose (%) | 6.18 (0.9) | 6.54 (0.4) | 6.78 (1.5) | 6.07 (0.4) | 6.01 (0.3) | 6.13 (0.3) | ns |
Non-fat dry matter content (%) | 7.8 (0.5) | 8.65 (0.2) | 8.04 (1.4) | 7.23 (0.3) | 7.31 (0.5) | 7.35 (0.2) | ns |
Total solids (%) | 9.03 (0.5) | 9.50 (0.4) | 9.18 (1.9) | 8.73 (0.5) | 8.37 (0.4) | 8.69 (0.4) | ns |
Ash (%) | 0.413 (0.09) | 0.385 (0.012) | 0.428 (0.011) | 0.343 (0.016) | 0.372 (0.025) | 0.438 (0.080) | ns |
C1 | C2 | C3 | C4 | C5 | A1 | p < 0.05 | |
---|---|---|---|---|---|---|---|
TAMC | 2.18 (0.9) | 2.38 (0.4) | 2.54 (0.4) | 2.55 (0.1) | 2.71 (0.5) | 2.37 (0.4) | ns |
LAB | 1.67 (0.9) | 0.99 (0.1) | 1.19 (0.8) | 1.38 (0.8) | 1.45 (0.2) | 1.18 (0.8) | ns |
Lactococci | 2.56 (0.2) | 1.95 (0.6) | 1.84 (0.2) | 1.76 (0.3) | 2.35 (0.1) | 1.83 (0.2) | ns |
Enterococci | 0.58 (0.7) | 0.50 (0.9) | 0.74 (1.4) | 0.89 (0.6) | 0.77 (0.9) | 0.22 (0.2) | ns |
Psychrotrophic bacteria | 1.48 (1.4) | 2.34 (0.9) | 2.37 (0.8) | 1.48 (0.9) | 2.36 (0.8) | 1.83 (0.8) | ns |
Micrococci | 2.86 (0.5) | 1.85 (1.2) | 2.18 (0.9) | 2.45 (0.3) | 2.70 (0.9) | 2.33 (0.5) | ns |
Coliforms | 1.86 (0.6) | 1.29 (1.2) | 2.18 (0.9) | 1.92 (0.8) | 1.50 (0.7) | 1.08 (0.1) | ns |
Υeasts/moulds | 2.56 (0.3) | 2.95 (1.2) | 1.86 (0.6) | 2.42 (0.1) | 2.54 (0.8) | 2.56 (0.3) | ns |
Clostridium spp. | 1.23 (0.8) | 1.18 (0.4) | 2.18 (0.9) | 1.36 (0.1) | 1.99 (0.8) | 1.13 (1.2) | ns |
Bacillus cereus | 1.53 (1.3) | 1.73 (1.4) | 2.18 (0.9) | 1.15 (0.8) | 1.32 (0.9) | 1.12 (0.9) | ns |
SCC | 4.40 (0.09) | 4.32 (0.10) | 4.05 (0.20) | 4.22 (0.08) | 3.92 (0.12) | 3.79 (0.31) | ns |
Isolate Number 1 | Closest Relative | Identity (%) | Accession Number |
---|---|---|---|
C1.2 | St. aureus | 99 | CP009361 |
C4.24 | Ec. mundtii | 94 | KM005159 |
C1.32 | Ec. mundtii | 99 | KM005159 |
C1.33 | Lb. brevis | 99 | KC713915 |
A1.39 | Ec. mundtii | 99 | KM005159 |
C2.46 | Lb. brevis | 98 | KC713915 |
C2.48 | Lb. brevis | 97 | KJ994501 |
C2.49 | Lb. brevis | 99 | KJ994501 |
C2.50 | Lb. brevis | 99 | KC713915 |
C4.51 | Lb. brevis | 97 | KJ994501 |
C5.56 | Lb. brevis | 99 | KC713915 |
C5.59 | Lb. brevis | 99 | KC713915 |
C4.67 | Ln. mesenteroides | 99 | JQ800447 |
C4.70 | Lc. lactis | 99 | KJ958440 |
C4.71 | Lc. lactis | 99 | KJ958440 |
C4.72 | Str. macedonicus | 98 | AF459431 |
A1.74 | Ec. faecalis | 99 | HF558530 |
A1.75 | Ec. durans | 99 | KJ958437 |
C3.76 | Ec. faecium | 99 | KJ832070 |
C3.77 | Ec. durans | 99 | KJ702532 |
C2.78 | Ec. durans | 100 | KF250785 |
C2.79 | Ec. durans | 99 | KF250827 |
C2.80 | Ec. faecium | 99 | KJ958432 |
C3.81 | Str. macedonicus | 99 | JX850868 |
Bacteria Species | C1 | C2 | C3 | C4 | C5 | A1 |
---|---|---|---|---|---|---|
Ec. durans | 2 (3) | 1 (2) | 1 (2) | |||
Ec. faecalis | 1 (3) | |||||
Ec. faecium | 1 (2) | 1 (1) | ||||
Ec. mundtii | 4 (6) | 2 (3) | 1 (2) | 2 (3) | ||
Lb. brevis | 3 (5) | 5 (7) | 2 (3) | 2 (4) | 3 (5) | |
Lc. lactis | 4 (11) | 4 (9) | ||||
Ln. mesenteroides | 1 (3) | |||||
St. aureus | 4 (4) | 2 (2) | 1 (1) | |||
Str. macedonicus | 1 (2) | 1 (2) |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Massouras, T.; Bitsi, N.; Paramithiotis, S.; Manolopoulou, E.; Drosinos, E.H.; Triantaphyllopoulos, K.A. Microbial Profile Antibacterial Properties and Chemical Composition of Raw Donkey Milk. Animals 2020, 10, 2001. https://doi.org/10.3390/ani10112001
Massouras T, Bitsi N, Paramithiotis S, Manolopoulou E, Drosinos EH, Triantaphyllopoulos KA. Microbial Profile Antibacterial Properties and Chemical Composition of Raw Donkey Milk. Animals. 2020; 10(11):2001. https://doi.org/10.3390/ani10112001
Chicago/Turabian StyleMassouras, Theofilos, Nefeli Bitsi, Spiros Paramithiotis, Eugenia Manolopoulou, Eleftherios H. Drosinos, and Kostas A. Triantaphyllopoulos. 2020. "Microbial Profile Antibacterial Properties and Chemical Composition of Raw Donkey Milk" Animals 10, no. 11: 2001. https://doi.org/10.3390/ani10112001
APA StyleMassouras, T., Bitsi, N., Paramithiotis, S., Manolopoulou, E., Drosinos, E. H., & Triantaphyllopoulos, K. A. (2020). Microbial Profile Antibacterial Properties and Chemical Composition of Raw Donkey Milk. Animals, 10(11), 2001. https://doi.org/10.3390/ani10112001