Microbiological Quality of Typical Traditional Fermented Milk from Northern Uganda and Western Kenya
Abstract
:1. Introduction
2. Materials and Methods
2.1. Collection of Samples
2.2. Sample Analysis
2.2.1. pH Measurement
2.2.2. Titratable Acidity of Fermented Milk Sample
- Vt = volume of titrant (ml NaOH).
- N = normality of titrant.
- 90 = equivalent weight for lactic acid.
- Vs = volume of sample used (ml yoghurt/milk).
2.3. Isolation of Microorganisms
2.3.1. Sample Preparations
2.3.2. Isolation of Microorganisms
- (i)
- Plate count agar (Oxoid M325, Basingstoke, Hampshire, UK), incubated in an inverted position at 30 ± 1 °C for 48–72 ± 1 h [28], for enumeration of total aerobic plate counts. This estimates the number of viable aerobic bacteria per gramme, or millilitre of the product measured, in colony-forming units per ml (cfu/mL) [29]. Plates that contained 30 to 300 colonies were counted.
- (ii)
- de Man Rogosa and Sharpe agar [30] (MRS, LAB098 pH 5.5) incubated anaerobically for 48 ± 2 h at 42 ± 1 °C in anaerobic jars (Biolab and Oxoid) with gas generating kits (Oxoid BR 38B) for selective enumeration of thermophilic lactobacilli, particularly Lactobacillus delbrueckii subsp. Bulgaricus.
- (iii)
- Rogosa agar [31] (E. Merck, D-61 Darmstadt, Germany), incubated anaerobically for 48 ± 2 h at 35 ± 1 °C, for enumeration of mesophilic lactobacilli. A further analysis was performed on MRS agar + vancomycin for the enumeration of Leuconostocs incubated anaerobically at 32 °C for 48 ± 2 h.
- (iv)
- M17 agar [32] (Oxoid CM 0817, pH 6.5), incubated aerobically for 48 ± 2 h at 30 ± 1 °C for the enumeration of lactococci, especially Streptococcus thermophilus. Ten isolates were obtained randomly from the countable plates of MRS, M17, and Rogosa agars, incubated at 42 °C for thermophilic bacteria and at 35 °C for mesophilic bacteria. Isolates were cultivated in MRS broth (CM359) pH 5.5 and pH 6.5 at 37 °C for 48–72 h for selective enumeration of Streptococcus thermophilus, Lactobacillus delbrueckii subsp. Bulgaricus, Lactobacillus acidophilus, Lactobacillus casei, and Bifidobacterium.
- (v)
- Xylose lysine deoxycholate (XLD) agar for the enumeration of Salmonella and Shigella spp. A 25 mL portion of the sample was pre-enriched with 225 mL of buffered peptone water and incubated for 24 h at 37 °C. A portion (0.1 mL) of the pre-enriched culture was transferred to 9.9 mL of Rappaport-Vassiliadis broth and incubated at 42 °C for 24 h. A loopful of the enrichment broth was then transferred to XLD agar and incubated at 37 °C for 24 h. Characteristic Salmonella colonies that each showed a slightly transparent zone of reddish colour and black centre were sub-cultured on nutrient agar and confirmed biochemically using triple sugar iron and Simon citrate agar according to the procedures of Gebeheyu et al. [11], with some modification.
- (vi)
- Violet red bile agar (Oxoid CM 107 with added 4-methylumbelliferyl-β-D-glucuronide (MUG) supplement BRO 71 E), incubated aerobically for 24 ± 2 h at 37 ± 1 °C for enumeration of non-sorbitol E. coli. The use of the supplement that contained MUG enabled the separate enumeration of E. coli that show glucuronidase activity. Plates were examined under long-wave UV light (366 nm) for the presence of fluorescing colonies. The presence of E. coli was tested further using indole production in tryptone water (Oxoid, UK) with Kovac’s reagent (Biolife, Sarasota, FL, USA), according to AOAC methods [29], and as previously reported by Moushumi and Prabir [33]. Further analysis of total coliform was performed using violet, red bile lactose agar incubated aerobically for 24 + 2 h at 30 ± 1 °C. Only plates containing 15 to 150 colonies for coliform were counted.
- (vii)
- Bacillus cereus was enumerated through the use of the most probable number technique with the selective agar mannitol yolk polymyxin B and polymyxin pyruvate egg mannitol bromothymol blue [29].
- (viii)
- (ix)
- A listeria-selective medium was used for the enumeration of L. monocytogenes. The International Dairy Federation method [17] was used. A 25 mL sample was homogenised in 225 mL of listeria enrichment broths A and B, and then incubated for 24 h at 37 °C on listeria-selective medium (Oxford formulation CM856, Oxoid™, UK) adjunct with listeria-selective supplement (SR0140, Oxoid™, UK). The latter was then incubated for 48 h at 30 °C. A loopful of the enrichment culture broth was streaked in duplicate onto polymyxin acriflavine lithium chloride ceftazidime aesculin mannitol agar (Oxoid, CM877) and incubated for 48 h at 37 °C. Suspected L. monocytogenes colonies were characterised through the use of the Gram staining and catalase test. Five presumptive L. monocytogenes colonies were selected from each Petri dish of selective agar and cultivated on trypticase soy agar medium (CM0131, Oxoid, UK) that had been supplemented with 0.6% yeast extract. They were placed subsequently into an incubator for 24 h at 30 °C. Listeria spp. Colonies typically ranged from greyish green to brownish green with black zones of 1–3 mm diameter of aesculin hydrolysis.
- (x)
- Malt extract agar (1.5% agar no 2) (Oxoid) and potato dextrose agar (+0.005 g/L chloramphenicol) were used to enumerate yeast and mould counts. The plates were incubated at 20 and 25 ± 1 °C for five days. Yeasts and mould colonies were counted separately. Plates that contained 10 to 200 yeast and mould colonies were counted [36].
2.4. Analytical Profile Index Biochemical Test
2.5. Data Analysis
3. Results
3.1. pH and TA
3.2. Microbial Counts
3.3. Microbial Analysis
3.3.1. Identification of the Isolates with API Biochemical Analysis
3.3.2. Yeast and Mould
3.4. Survival of Pathogens during Storage
4. Discussion
5. Conclusions
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Materia, V.C.; Linnemann, A.R.; Smid, E.J.; Schoustra, S.E. Contribution of traditional fermented foods to food systems transformation: Value addition and inclusive entrepreneurship. Food Secur. 2021, 13, 1163–1177. [Google Scholar] [CrossRef]
- Iwuoha, C.I.; Eke, O.S. Nigerian indigenous fermented foods: Their traditional process operation, inherent problems, improvements and current status. Food Res. Int. 1996, 29, 527–540. [Google Scholar] [CrossRef]
- Moatsou, G.; Moschopoulou, E. Microbiology of Raw Milk. In Dairy Microbiology and Biochemistry: Recent Developments; Özer, B.H., Akdemir-Evrendilek, G., Eds.; Taylor & Francis Group, LLC: New York, NY, USA, 2015; pp. 1–38. [Google Scholar]
- Aliyo, A.; Teklemariam, Z. Assessment of Milk Contamination, Associated Risk Factors, and Drug Sensitivity Patterns among Isolated Bacteria from Raw Milk of Borena Zone. Ethiop. J. Trop. Med. 2022, 2022, 3577715. [Google Scholar] [CrossRef]
- Yambayamba, K.E.; Zulu, M.P. Influence of the milking environment on the microbial quality of raw milk produced by smallholder farmers in Magoye. UNZA J. Sci. Technol. 2011, 15, 37–43. [Google Scholar]
- Leone, C.; Thippareddi, H.; Ndiaye, C.; Niang, I.; Diallo, Y.; Singh, M. Safety and Quality of Milk and Milk Products in Senegal—A Review. Foods 2022, 11, 3479. [Google Scholar] [CrossRef] [PubMed]
- Moonga, H.B. Product Optimization of Zambian Traditionally Fermented Milk-Mabisi. Doctoral Dissertation, Wageningen University, Wageningen, The Netherlands, 2019. [Google Scholar]
- Maleke, M.S.; Adefisoye, M.A.; Doorsamy, W.; Adebo, O.A. Processing, nutritional composition, and microbiology of amasi: A Southern African fermented milk product. Sci. Afr. 2021, 12, e00795. [Google Scholar] [CrossRef]
- Landis, E.A.; Oliverio, A.M.; McKenney, E.A.; Nichols, L.M.; Kfoury, N.; Biango-Daniels, M.; Shell, L.K.; Madden, A.A.; Shapiro, L.; Sakunala, S.; et al. The diversity and function of sourdough starter microbiomes. eLife 2021, 10, e61644. [Google Scholar] [CrossRef]
- Mazurek, J.; Salehi, E.; Propes, D.; Holt, J.O.; Bannerman, T.; Nicholson, L.M.; Bundesen, M.; Duffy, R.; Moolenaar, R.L. A multistate outbreak of Salmonella enterica serotype Typhimurium infection linked to raw milk consumption—Ohio, 2003. J. Food Prot. 2004, 67, 2165–2170. [Google Scholar] [CrossRef]
- Gebeyehu, A.; Taye, M.; Abebe, R. Isolation, molecular detection and antimicrobial susceptibility profile of Salmonella from raw cow milk collected from dairy farms and households in southern Ethiopia. BMC Microbiol. 2022, 22, 84. [Google Scholar] [CrossRef]
- Chatti, A.; Daghfous, D.; Landoulsi, A. Acid resistance of Salmonella isolated from animals, food and wastewater in Tunisia. Ann. Saudi Med. 2007, 27, 195–198. [Google Scholar] [CrossRef]
- Massa, S.; Altieri, C.; Quaranta, V.; De Pace, R. Survival of Escherichia coli O157: H7 in yoghurt during preparation and storage at 4 °C. Lett. Appl. Microbiol. 1997, 24, 347–350. [Google Scholar] [CrossRef]
- Conner, D.; Kotrola, J.S. Growth and survival of Escherichia coli O157:H7 under acidic conditions. Appl. Environ. Microbiol. 1995, 61, 382–385. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ogwaro, B.A.; Gibson, H.; Whitehead, M.; Hill, D.J. Survival of Escherichia coli O157:H7 in traditional African yoghurt fer-mentation. Int. J. Food Microbiol. 2002, 79, 105–112. [Google Scholar] [CrossRef]
- Bashiry, M.; Javanmardi, F.; Taslikh, M.; Sheidaei, Z.; Sadeghi, E.; Abedi, A.S.; Mirza Alizadeh, A.; Hashempour-Baltork, F.; Beikzadeh, S.; Riahi, S.M.; et al. Listeria monocytogenes in Dairy Products of the Middle East Region: A Systematic Review, Meta-Analysis, and Meta-Regression Study. Iran J. Public Health 2022, 51, 292–305. [Google Scholar] [CrossRef]
- Motarjemi, Y.; Moy, M.G.G.; Jooste, P.J.; Anelich, L.E. Milk and Dairy Products. Chapter 5. In Food Safety Management; Elsevier: Amsterdam, The Netherlands, 2014; pp. 83–117. [Google Scholar]
- Sanaa, M.; Poutrel, B.; Menard, J.L.; Serieys, F. Risk factors associated with contamination of raw milk by Listeria monocytogenes in dairy farms. J. Dairy Sci. 1993, 76, 2891–2898. [Google Scholar] [CrossRef] [PubMed]
- Le Loir, Y.; Baron, F.; Gautier, M. Staphylococcus aureus and food poisoning. Genet. Mol. Res. 2003, 2, 63–76. [Google Scholar]
- Pazakova, J.; Turek, P.; Laciakova, A. The survival of Staphylococcus aureus during the fermentation and storage of yoghurt. J. Appl. Microbiol. 1997, 82, 659–662. [Google Scholar] [CrossRef] [PubMed]
- Umoh, V.J.; Adesiyun, A.A.; Gomwalk, N.E. The occurrence of Staphylococcus aureus in fermented milk products (fura and manshanu) in Nigeria. Int. J. Food Microbiol. 1990, 10, 343–347. [Google Scholar] [CrossRef]
- Peton, V.; Le Loir, Y. Staphylococcus aureus in veterinary medicine. Infect. Genet. Evol. 2014, 21, 602–615. [Google Scholar] [CrossRef] [PubMed]
- Tirloni, E.; Stella, S.; Celandroni, F.; Mazzantini, D.; Bernardi, C.; Ghelardi, E. Bacillus cereus in Dairy Products and Production. Plants Foods 2022, 11, 2572. [Google Scholar] [CrossRef]
- Washaya, S.; Jakata, C.; Tagwira, M.; Mupofu, T. Bacterial Milk Quality along the Value Chain in Smallholder Dairy Production. Sci. World J. 2022, 21, 7967569. [Google Scholar] [CrossRef]
- Obafemi, Y.D.; Oranusi, S.U.; Ajanaku, K.O.; Akinduti, P.A.; Leech, J.; Cotter, P.D. African fermented foods: Overview, emerging benefits, and novel approaches to microbiome profiling. npj Sci Food. 2022, 6, 15. [Google Scholar] [CrossRef] [PubMed]
- Nyambane, B.; Thari, W.M.; Wangoh, J.; Njage, P.M.K. Lactic acid bacteria and yeasts involved in the fermentation of amabere amaruranu, a Kenyan fermented milk. Food Sci. Nutr. 2014, 2, 692–699. [Google Scholar] [CrossRef] [PubMed]
- Mukisa, I.M.; Kyoshabire, R. Microbiological, physicochemical, and sensorial quality of small-scale produced stirred yoghurt on the market in Kampala city, Uganda. Nutr. Food Sci. 2010, 40, 409–418. [Google Scholar] [CrossRef]
- EN ISO 8261:2001; Milk and Milk Products-General Guidance for the Preparation of Test Samples, Initial Suspensions and Decimal Dilutions for Microbiological Examination: Lait et Produits Laitiers-Lignes Directrices Générales Pour la Préparaton des Échantillons Pour Essai, de la Suspension Mère et Des Dilutions Décimales en Vue de L’e-xamen Microbiologique. IOS (International Organization for Standardization): Geneva, Switzerland, 2001.
- Association of Official Analytical Chemist. Official Methods of Analysis, 18th ed.; Association of Official Analytical Chemist: Washington, DC, USA, 2006. [Google Scholar]
- De Man, J.C.; Rogosa, M.; Sharpe, E.M. A medium for the cultivation of Lactobacilli. J. App. Bact. 1960, 23, 130–135. [Google Scholar] [CrossRef]
- Rogosa, M.; Mitchell, J.A.; Wiseman, R.F. A selective medium for the isolation of oral and faecal lactobacilli. J. Bacteriol. 1951, 62, 132–133. [Google Scholar] [CrossRef] [Green Version]
- Terzaghi, B.E.; Sandine, W.E. Improved medium for lactic Streptococci and their bacteriophages. Appl. Microb. 1975, 29, 807–813. [Google Scholar] [CrossRef]
- Moushumi, B.; Prabir, K.S. Microbiological quality of some retail spices in India. Food Res. Int. 2003, 36, 469–474. [Google Scholar]
- International Dairy Federation. Milk and Milk-Based Products—Enumeration of Staphylococcus Aureus (IDF Standard 1990); IDF145; IDF: Schaerbeek, Brussels, 1990. [Google Scholar]
- ISO 6888-1:2021; Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for the Enumeration of Coagulase-Positive Staphylococci (Staphylococcus aureus and Other Species)—Part 1: Method Using Baird-Parker Agar Medium. ISO (International Organization for Standardization): Geneva, Switzerland, 2021.
- Duncan, S.; Yaun, E.; Sumner, S.S.; Bruhn, J. Chapter 09 Microbiological Methods for Dairy Products. In Standard Methods for the Examination of Dairy Products; American Public Health Association: Washington, DC, USA, 2012. [Google Scholar] [CrossRef]
- Reiner, K. Catalase Test Protocol; American Society Microbiology: Washington, DC, USA, 2016. [Google Scholar]
- Sulaiman, I.M.; Hsieh, Y.H. Foodborne Pathogens in Milk and Dairy Products: Genetic Characterization and Rapid Diagnostic Approach for Food Safety of Public Health Importance. In Dairy in Human Health and Disease across the Lifespan; Springer: Berlin, Germany, 2017; pp. 127–143. [Google Scholar]
- Makut, D.; Ogbonna, A.I.; Dalami, H. An Assessment of the Bacteriological Quality of Different Brands of Yoghurt Sold in Keffi, Nasarawa State, Nigeria. J. Nat. Sci. Res. 2014, 4, 19–22. [Google Scholar]
- Nduko, J.M.; Matofari, J.W.; Nandi, Z.O.; Sichangi, M.B. Spontaneously fermented Kenyan milk products. A review of the current state and future perspectives. Afr. J. Food Sci. 2017, 11, 1–11. [Google Scholar]
- Ifeanyi, V.O.; Ihesiaba, E.O.; Muomaife, O.M.; Ikenga, C. Assessment of microbiological quality of yoghurt sold by street vendors in Onitsha metropolis, Anambra State, Nigeria. Br. Microbiol. Res. J. 2013, 3, 198. [Google Scholar] [CrossRef] [Green Version]
- Digbabul, B.; Shember, J.; Amove, J. Physicochemical, microbiological, and sensory evaluation of yoghurt sold in Makurdi me-tropolis. Afr. J. Food Sci. Technol. 2014, 5, 129–135. [Google Scholar]
- Health Protection Agency (HPA). Guidelines for Assessing the Microbiological Safety of Ready-to-Eat Foods; Health Protection Agency: London, UK, 2009.
- Majoie, G.Ã.; Mousse, W.; Haziz, S.I.N.; Farid, B.A.D.; Ahouissou, O.R.; Adjanohoun, A.; Lamine, B.M. Microbial quality of artisanal yoghurt and Degue products collected in schools of Cotonou and Abomey-Calavi (Benin) Afr. J. Food Sci. 2020, 14, 112–118. [Google Scholar]
- Jans, C.; Meile, L.; Kaindi, D.W.; Kogi-Makau, W.; Lamuka, P.; Renault, P.; Kreikemeyer, B.; Lacroix, C.; Hattendorf, J.; Zinsstag, J.; et al. African fermented dairy prod-ucts–overview of predominant technologically important microorganisms focusing on African Streptococcus infantarius var-iants and potential future applications for enhanced food safety and security. Int. J. Food Microbiol. 2017, 250, 27–36. [Google Scholar] [CrossRef]
- Abdalla, M.O.M.; Abdel Nabi, S.Z. Evaluation of microbiological quality of Sudanese fermented dairy product ‘mish’ during storage. Adv. J. Food Sci. Tech. 2010, 2, 155–158. [Google Scholar]
- Moonga, H.B.; Schoustra, S.E.; Linnemann, A.R.; Kuntashula, E.; Shindano, J.; Smid, E.J. The art of mabisi production: A traditional fermented milk. PLoS ONE 2019, 14, e0213541. [Google Scholar] [CrossRef] [Green Version]
- Benkirane, G.; Ananou, S.; Dumas, E.; Ghnimi, S.; Gharsallaoui, A. Moroccan Traditional Fermented Dairy Products: Current processing Practices and Physiochemical and Microbiological Properties: A Review. J. Microbiol. Biotechnol. Food Sci. 2022, 12, e5636. [Google Scholar] [CrossRef]
- Doslash, R.; Osvik, V.; Sperstad, S.; Breines, E.; Hareide, E.; Godfroid, J.; Zhou, Z.; Ren, P.; Geoghegan, C.; Holzapfel, W.; et al. Bacterial Diversity of aMasi, a South African Fermented Milk Product, Determined by Clone Library and Denaturing Gradient Gel Electrophoresis Analysis. AJMR 2013, 7, 4146–4158. [Google Scholar] [CrossRef]
- Taye, Y.; Degu, T.; Fesseha, H.; Mathewos, M. Isolation and Identification of lactic acid bacteria from cow Milk and Milk products. Sci. World J. 2021, 2021, 4697445. [Google Scholar] [CrossRef]
- Gleeson, D.; O’Brien, B.; Flynn, J.; O’Callaghan, E.; Galli, F. Effect of pre-milking teat preparation procedures on the microbial count on teats prior to cluster application. Ir. Vet. J. 2009, 62, 461. [Google Scholar] [CrossRef] [Green Version]
- Haile, W.; Yilma, Z.; Teklegiorgis, Y. Incidence of pathogenic and indicator bacteria in raw and pasteurized milk in Hawassa city, rift valley of Southern Ethiopia. Afr. J. Food Sci. 2012, 7, 100–107. [Google Scholar]
- Ismail Ahmed, A. Isolation and Identification of LAB from Sudanese Traditional Fermented Camel (Camelus dromedarius) Milk Gariss. Open J. Nutr. Food Sci. 2022, 4, 1022. [Google Scholar]
- Obodai, M.; Dodd, C.E.R. Characterization of dominant microbiota of a Ghanaian fermented milk product, nyarmie, by cul-ture- and nonculture-based methods. J. Appl. Microbiol. 2006, 100, 1355–1363. [Google Scholar] [CrossRef] [PubMed]
- Owusu-Kwarteng, J.; Tano-debrah, K.; Glover, R.L.K.; Akabanda, F. Process characteristics and microbiology of fura produced in Ghana. Nat. Sci. 2010, 8, 41–51. [Google Scholar]
- Mathara, J.M.; Schillingera, U.; Kutima, P.M.; Mbugua, S.K.; Holzapfel, W.H. Isolation, Identification, and characterisation of the dominant microorganisms of kule naoto: The Maasai traditional fermented milk in Kenya. Int. J. Food Microbiol. 2004, 94, 269–278. [Google Scholar] [CrossRef]
- Teuber, M. The Genus Lactococcus. In The Genera of Lactic Acid Bacteria. The Lactic Acid Bacteria; Wood, B.J.B., Holzapfel, W.H., Eds.; Springer: Boston, MA, USA, 1995; Volume 2. [Google Scholar]
- Togo, C.A.; Feresu, S.B.; Mutukumira, A.N. Identification of Lactic Acid Bacteria isolated from Opaque beer (Chibuku) for potential use as a starter culture. J. Food Technol. Afr. 2002, 7, 93–97. [Google Scholar] [CrossRef] [Green Version]
- Hamama, A. Moroccan Traditional Fermented Dairy Products. In Applications of Biotechnology to Traditional Fermented Foods; Ruskin, F.R., Ed.; National Academy Press: Washington, DC, USA, 1992; pp. 75–79. [Google Scholar]
- Foster, J.W. Low pH Adaptation and the Acid—Tolerance Response of Salmonella typhimurium. Crit. Rev. Microbiol. 2008, 21, 215–237. [Google Scholar] [CrossRef]
- Liyuwork, T.; Biruhalem, T.; Sefinew, A.; Hailleleul, N. Prevalence and antimicrobial resistance profile of Salmonella isolates from dairy products in Addis Ababa, Ethiopia. Afr. J. Microbiol. Res. 2013, 7943, 5045–5050. [Google Scholar]
- Bereda, A.; Yesuf Kurtu, M.; Yilma, Z. Handling, processing and utilization of Milk and Milk products in Ethiopia: A review. World J. Dairy Food Sci. 2014, 9, 105–112. [Google Scholar]
- Pyz-Lukasik, R.; Paszkiewicz, W.; Brodzki, P.; Belkot, Z. Microbiological quality of milk sold directly from producers to con-sumers. J. Dairy Sci. 2015, 98, 4294–4301. [Google Scholar] [CrossRef] [Green Version]
- Fleet, G.H. Yeasts in dairy products. A Review. J. Appl. Bacteriol. 1990, 68, 199–211. [Google Scholar] [CrossRef] [PubMed]
- Akabanda, F.; Owusu-Kwarteng, J.; Glover, R.L.K.; Tano-Debrah, K. Microbiological characteristics of Ghanaian traditional fermented milk product. Nunu. Nat. Sci. 2010, 8, 178–187. [Google Scholar]
- Savova, L.; Nikolova, M. Isolation and Taxonomic study of yeast strain from Bulgarian Dairy products. J. Cult. Collect. 2000, 3, 59–65. [Google Scholar]
- Getachew, A.; Tadie, A.; Chercos, D.H.; Guadu, T. Level of Faecal Coliform Contamination of Drinking Water Sources and Its Associated Risk Factors in Rural Settings of North Gondar Zone, Ethiopia: A Cross-Sectional Community Based Study. Ethiop. J. Health Sci. 2018, 28, 227–234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bùchi, N.R.; Seller, H. Yeast and moulds: Yeasts in milk and dairy products. In Encyclopedia of Dairy Sciences, 2nd ed.; Academic Press: Cambridge, MA, USA, 2011; pp. 744–753. [Google Scholar] [CrossRef]
- International Commission on Microbiological Specifications for Foods. Microorganisms in Foods 5: Microbiological Specifications of Food Pathogens; Blackie Academic and Professional: New York, NY, USA, 1996; p. 6. [Google Scholar]
- Food and Agriculture Organisation of the United Nations (FAO). Guide to Good Dairy Farming Practice: Milking Hygiene; Food and Agriculture Organisation of the United Nations (FAO): Rome, Italy, 2023. [Google Scholar]
No. | Medium for Growth | Microorganisms | Time (hour) | Growth Condition and Incubation Temperature (°C) |
---|---|---|---|---|
i | Plate count agar (Oxoid M325) | Total aerobic mesophilic bacteria | 48 ± 2 | aerobic 30 ± 1 |
ii | MRS agar (LAB098) (pH 6.5) | Mesophilic lactobacilli | 48 ± 2 | aerobic 35 ± 1 |
iii | Rogosa agar | Mesophilic lactobacilli | 48 ± 2 | anaerobic 35 ± 1 |
iv | MRS agar (LAB 098 + vancomycin) | Leuconostoc | 48 ± 2 | anaerobic 30 ± 1 |
V | MRS agar (pH 5.5) (LAB098) | Thermophilic lactobacilli | 48 ± 2 | anaerobic 42 ± 1 |
vii | MRS agar (pH 6.0) (LAB098) | Thermophilic lactococci | 48 ± 2 | anaerobic 42 ± 1 |
viii | M17 agar (LAB 092) | Streptococci | 48 ± 2 | anaerobic 30 ± 1 |
viii | Violet red bile lactose agar with MUG supplement BRO 71 E), | Non-sorbitol E. coli | 24 ± 2 | aerobic 37 ± 1 |
ix | Violet red bile agar | Coliform | 24 ± 2 | aerobic 30 ± 1 |
X | XLD | Salmonella and Shigella spp. | 24 ± 2 | aerobic 37 ± 1 |
xi | Baird-Parker’s medium (Oxoid CM 0275 + SR054C) | Staphylococcus aureus | 24 ± 2 | aerobic 37 ± 1 |
xii | Listeria enrichment broths A and B | Listeria monocytogenes | 24 ± 2 | aerobic 30 ± 1 |
xiii | Bacillus cereus agar | Bacillus cereus | 24 ± 2 | aerobic 30 ± 1 |
xiv | 1.5% malt extract and agar no. 2 | Yeasts | 120 ± 2 | aerobic 25 ± 1 |
xv | PDA + chloramphenicol | Mould | 120 ± 2 | aerobic 30 ± 1 |
Sample | pH | TA (%) |
---|---|---|
UG 1 | 2.9 ± 0.01 | 1.26 ± 0.1 |
UG 2 | 3.4 ± 0.01 | 0.71 ± 0.1 |
KE | 3.6 ± 0.01 | 0.92 ± 0.1 |
No. | Microorganism | UG 1 | UG 2 | KE |
---|---|---|---|---|
i | Total aerobic mesophilic bacterial counts | 9.35 | 9.68 | 9.69 |
ii | Mesophilic lactobacilli (aerobic) | 7.24 | 7.28 | 7.28 |
iii | Mesophilic lactobacilli (anaerobic) | 7.8 | 6.33 | 7.28 |
iv | Leuconostoc | 5.77 | 5.68 | 5.70 |
v | Mesophilic lactococci | 7.94 | 8.20 | 8.32 |
vi | Thermophilic lactobacilli. | 8.23 | 8.29 | 8.32 |
vii | Thermophilic lactococci | 7.85 | 7.76 | 7.76 |
viii | Streptococci | 8.22 | 8.02 | 8.02 |
ix | Non-sorbitol E. coli | 4.08 | 3.34 | 3.34 |
x | Coliform | 5.33 | 4.33 | 4.24 |
xi | Salmonella spp. | 2.97 | 2.87 | 2.93 |
xii | Shigella spp. | 0.00 | 0.00 | 0.00 |
xiii | Staphylococcus aureus | 4.41 | 4.35 | 4.11 |
xiv | Listeria monocytogenes | 1.18 | 1.13 | 1.12 |
xv | Bacillus cereus | 2.92 | 2.86 | 2.82 |
xvi | Yeasts | 8.33 | 8.36 | 8.52 |
xvii | Mould | 8.04 | 8.17 | 8.21 |
Isolate | Macro-Colony Morphology (Margin, Colour, Elevation, Cell Appearance) | UG1 | UG2 | KE |
---|---|---|---|---|
1 | Cream, smooth, oval shape entire and ellipsoidal cell | √ | √ | √ |
2 | Undulating, white top with green base, slightly convex, spheroidal to short ellipsoidal. (Blue colony on Kluveymyces differential medium) | √ | √ | √ |
3 | Yellow-green, powdery and pale yellowish on reverse Aspergillus flavus | √ | ND | √ |
4 | Dirty white with yellow spores at the centre, base orange, slightly radially furrowed (Microsporum spp.). | √ | √ | √ |
5 | Cream-yellow, powdery, and pale yellowish on reverse, capsulate margin, slightly raised centre, filamentous cells | √ | √ | √ |
6 | White to cream, yellowish, wrinkled, nearly flat elevation, oval cells and ellipsoidal | √ | √ | ND |
7 | White to cream coloured, flat with aerial mycelium (Aspergillus spp.) | √ | √ | √ |
8 | Green with a red base | √ | √ | √ |
9 | White at the base and black spores at the top | √ | √ | √ |
10 | White pin head, clear zones around the colony | √ | √ | √ |
11 | Black, yellow to pale cream in the centre (Aspergillus) | ND | ND | ND |
12 | White measuring 1–4 mm, opaque and flat. Ropy to the touch | √ | √ | √ |
13 | Straw cream at the centre, base orange, slightly radially furrowed | √ | √ | ND |
14 | Well-formed white colonies (Aspergillus spp.) | √ | √ | √ |
15 | Green and pale yellow on reverse (Penicillium) | ND | ND | ND |
16 | White base with black conidiophores | √ | ND | √ |
17 | Greenish black, white mycelia at the margin, white in the centre (Rhizopus sp.) | ND | ND | ND |
18 | Greenish surrounded by creamy-white ring at the margin (Penicillium) | ND | √ | ND |
19 | White to cream, smooth, glaucous dark green on the obverse and pale yellow on the reverse | ND | ND | ND |
20 | Cotton white to cream on the obverse and yellow to orange on the reverse with dark brown exudate | √ | √ | √ |
21 | White colony, opaque and flat | √ | √ | √ |
22 | Bright red colonies | ND | ND | ND |
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Ogwaro, B.A.; Gibson, H.; Hill, D.J.; O’Gara, E.A. Microbiological Quality of Typical Traditional Fermented Milk from Northern Uganda and Western Kenya. Dairy 2023, 4, 445-461. https://doi.org/10.3390/dairy4030030
Ogwaro BA, Gibson H, Hill DJ, O’Gara EA. Microbiological Quality of Typical Traditional Fermented Milk from Northern Uganda and Western Kenya. Dairy. 2023; 4(3):445-461. https://doi.org/10.3390/dairy4030030
Chicago/Turabian StyleOgwaro, Betty A., Hazel Gibson, Dave J. Hill, and Elizabeth A. O’Gara. 2023. "Microbiological Quality of Typical Traditional Fermented Milk from Northern Uganda and Western Kenya" Dairy 4, no. 3: 445-461. https://doi.org/10.3390/dairy4030030