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Owusu-kwarteng J, Akabanda F, Agyei D, Jespersen L. Microbial safety of Milk production and fermented dairy products in Africa. Microorganisms. 2020;8:1–24. In line with our findings, dirty barns [ 50], dirty cows [ 5, 56] and soiled udder and teats [ 16] were reported to be associated with increased CC in bulk milk. In this study, the use of warm water to clean teats was related to low CC. Similarly, a study conducted in Irish dairy herds reported an association between the use of heated water in the milking parlor and low bacterial counts [ 49]. The use of hot water is indicated to enhance washing efficacy [ 10]. CC is found to be significantly higher in peri-urban areas than in urban areas. This could be attributed to soil barn floor that can easily get muddy and low awareness on hygienic milk production practices. Millogo V, Sjaunja KS, Ouédraogo GA, Agenäs S. Raw milk hygiene at farms, processing units and local markets in Burkina Faso. Food Control. 2010;21:1070–4. Isaac P, Bohl LP, Breser ML, Orellano MS, Conesa A, Ferrero MA, Porporatto C. Commensal coagulase-negative Staphylococcus from the udder of healthy cows inhibits biofilm formation of mastitis-related pathogens. Vet Microbiol. 2017;207:259–66.
Cortimiglia C, Luini M, Bianchini V, Marzagalli L, Vezzoli F, Avisani D, Bertoletti M,Ianzano A,Franco A,Battisti A. Short Report. Prevalence of Staphylococcus aureus and of methicillin-resistant S. aureus clonal complexes in bulk tank milk from dairy cattle herds in Lombardy Region (Northern Italy). Epidemiol Infect. 2016;144:3046–51. van Schaik G, Green LE, Guzma’n D, Esparza H, Tadich N. Risk factors for bulk milk somatic cell counts and total bacterial counts in smallholder dairy farms in the 10th region of Chile. Prev Vet Med. 2005;67:1–17. Falentin H, Rault L, Nicolas A, Bouchard DS, Lassalas J, Lamberton P, Aubry J-M, Marnet P-G, Le Loir Y, Even S. Bovine teat microbiome analysis revealed reduced alpha diversity and significant changes in taxonomic profiles in quarters with a history of mastitis. Front Microbiol. 2016;7:480. Lima SF, Teixeira AG, Lima FS, Ganda EK, Higgins CH, Oikonomou G, Bicalho RC. The bovine colostrum microbiome and its association with clinical mastitis. J Dairy Sci. 2017;100:3031–42.Amenu K, Wieland B, Szonyi B, Grace D. Milk handling practices and consumption behavior among Borana pastoralists in southern Ethiopia. J Health Popul Nutr. 2019;6:1–12. Oliveira R, Pinho E, Almeida G, Azevedo NF, Almeida C. Prevalence and diversity of Staphylococcus aureus and staphylococcal enterotoxins in raw Milk from northern Portugal. Front Microbiol. 2022;13:846653. https://doi.org/10.3389/fmicb.2022.846653. Gonçalves JL, Kamphuis C, Martins CMMR, Barreiro JR, Tomazi T, Gameiro AH, Hogeveen H, Santos MV dos. Bovine subclinical mastitis reduces milk yield and economic return. Livest Sci. 2018;210:25–32. The result of this study showed that the occurrence of S. aureus in bulk milk (42%) was high compared to previous reports from other parts of Ethiopia [ 26, 28, 54, 74], Uganda [ 75], Brazil [ 76], the USA [ 17] and China [ 77]. Our finding complies with previous reports from Ethiopia [ 27], Greece [ 70] and Italy [ 78]. In contrast, slightly higher S. aureus-occurrences of 66, 61, 54, 51, 48% were reported in Brazil [ 15], India [ 58], Portugal [ 73], Ireland [ 49] and the USA [ 79], respectively. The high occurrence of S. aureus in this study is concerning because many strains can produce enterotoxins and consequently cause food-borne intoxication in consumers [ 32]. The high occurrence of S. aureus in bulk milk in this study could be indicative of mastitis in the studied farms. S. aureus might have also contaminated bulk milk from human handlers, milk utensils, the environment, and the udder and teat skin of dairy cows [ 78]. The absence of premilking teat preparation is a risk factor for the presence of S. aureus in bulk milk [ 15]. Thus, it is important that mastitis is prevented and hygienic milk production practices are implemented to safeguard the public from staphylococcal food poisoning [ 78]. A structured questionnaire survey was conducted to assess factors that thought to influence the hygienic quality of bulk milk. Farm owners were interviewed on their personal information, herd size, whether dairying primary income, experience in dairying in years, training on hygienic milk production, use of warm water and/or detergent for milk utensil cleaning, use of warm water for teat washing, smoking of milk utensils, raw milk consumption habits and education level. When an activity had been performed by a hired laborer or a family member other than the farm owner, they were interviewed on that specific activity. For example, activities such as milking, and cleaning practices. Data on factors such as hygiene of the barn/cows/udder/milkers, hygiene of milk utensil, cow shade roof type, material of milk utensil, premilking udder preparation practices and milking procedures were collected by observation. The questionnaires were conducted face-to-face during the milking procedure. To avoid variation among individuals, the questionnaire survey was conducted by the first author of this paper (AD). The questions were originally written in English and translated into Afaan Oromo or Amharic languages when administered. Cow and udder hygiene scoring
European Commission. Corrigendum to Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004. Laying down specific hygiene rules for food of animal origin. Off J Eur Union. 2004:22–82. Bomar L, Brugger SD, Yost BH, Davies SS, Lemon KP. Corynebacterium accolens releases antipneumococcal free fatty acids from human nostril and skin surface triacylglycerols. mBio 7(1):e01725-15. This study aimed to investigate the temporal dynamics of the microbiota in the bovine udder. The ten cows used for this purpose were divided in two groups based on the level of SCC before the first sampling. Five of the cows (L1–L5) had a stable low SCC (< 100,000 SCC/mL) on the three days leading up to the first sampling, while the remaining five cows (H1–H5) had a higher SCC (> 100,000 SCC/mL) in the same period. Quarter milk samples were collected from all ten cows at six samplings during a period of five months (January to May). Of the 240 quarter samples that were collected, six were missing during collection and were not included in the analysis. To study the microbial composition of the 234 remaining samples, amplicon sequencing of the 16S rRNA genes were performed for all the samples. The average depth of sequencing was 49,093 sequences per sample before filtering and 18,880 sequences per sample after filtering. In total 9132 high quality SVs were obtained from 234 samples. 14 samples were filtered out of the analysis because they did not pass the quality filtering of the Dada2 pipeline used to analyse the 16S data after sequencing. Of the 9,132 high quality SVs, 6962 SVs were used for taxonomy search, and 553 SVs were successfully assigned to family level. 61 quarter samples were classified as having an IMI based on definition “A” from Dohoo et al. [ 23]. This definition states that a quarter sample where > 10 colonies are cultured per 0.1 mL is defined as having an IMI. Eighty-nine percent of these were from group H and 11% were from group L. A limit of 100,000 SCC/mL was selected to classify the quarter samples as high or low SCC during samplings. 30 quarter samples had high SCC, 204 low SCC, and 6 samples had no recorded SCC. Of the 30 samples with a recorded high SCC, 93% were from group H and 7% from group L. Other additional data about the health, parturition, and recorded mastitis were retrieved from the Norwegian Cattle Health Recording System (Additional file 1). No cows were recorded to have mastitis during the sampling period, while two cows (L1 and H2) were treated for mastitis caused by Streptococcus dysgalactiae and Streptococcus uberis, respectively, after this period. The samplings occurred between 19 and 193 days in milk for the 10 cows (Additional file 2). This period encompasses the early and mid-lactation stages. Five of the cows (H4, H5, L3, L4, L5) were in their first parturition, while the remaining five (H1, H2, H3, L1, L2) were in their second parturition. Diversity analysis of the quarter samples Marshall JC, Soboleva TK, Jamieson P, French NP. Estimating bacterial pathogen levels in New Zealand bulk tank milk. J Food Prot. 2016;79:771–80.Two consecutive petri dishes with colony counts between 30 and 300 per plate were considered for TBC, while plates that contained 10–100 and 15–300 colonies were considered for CC and CPS, respectively. Then, the bacterial count in the respective original sample was expressed as the number of colony forming units per ml (cfu/ml) of samples according to ISO 7218:2007 [ 43]. Isolation and identification of Staphylococcus aureus The detection of Staphylococcus or Corynebacterium in all quarter samples were consistent with other studies [ 2, 14, 15, 22]. The udder microbiota of the L-cows turned out to be highly dynamic and diverse with fluctuations between the relative abundance of genera from one sampling to the next. In the one case where an IMI was detected and accompanied by an increase in the relative abundance of Corynebacterium and Novosphingobium, a diverse microbiota composition had been reestablished by the next sampling. A different tendency was recorded for the H-cows. In quarters with an established IMI or a raised SCC due to dominance of one genus ( Staphylococcus or Corynebacterium), returning to a diverse microbiota composition turned out to be difficult, and the dominant genus was found to linger throughout the whole sampling period. Some quarters appear to be dominated by Corynebacterium or Staphylococcus, yet they were culture negative under both aerobic and anaerobic conditions and have therefore not been labeled as having an IMI. This inconsistency between the 16S data and the culturing results is likely due to the inability of laboratory culturing methods to cultivate all bacteria in a sample. The criteria used to define a quarter sample as IMI positive in this study was chosen to identify as many IMIs as possible. Whilst definition “A” from Dohoo et al. [ 23] certainly achieves this, it can also introduce false positives to the dataset. To make up for this it would have been prudent to include species identification after plating on blood agar as an additional screening method for quarters with IMI. ISO 4833:2003. Microbiology of food and animal feeding stuffs — horizontal method for the enumeration of microorganisms — Colony-count technique at 30°C. Geneva: International Organization for Standardization; 2003. Observation and palpation of the udder is essential but tends to detect only later or more severe mastitis cases.
Seyoum B, Kefyalew H, Abera B, Abdela N. Prevalence, risk factors and antimicrobial susceptibility test of Staphylococcus aureus in bovine cross breed Mastitic Milk in and around Asella town, Oromia regional state, Southern Ethiopia. Acta Trop. 2017. https://doi.org/10.1016/j.actatropica.2017.09.012. The study was conducted in Asella, Arsi zone, Oromia regional state, Ethiopia. Asella is located at a latitude and longitude of 7°57ˈN and 39°7ˈE, respectively. Asella is the capital of Arsi zone and is located 175 km southeast of Addis Ababa in a highland plateau region at an elevation of 2430 m above sea level. Asella is categorized as having a subtropical highland climate with an annual mean rainfall and temperature of 1100 mm and 15.47 °C, respectively. The area experiences a bimodal rainfall pattern, with a short rainy season occurring during March and April and a long rainy season extending from June to September [ 35]. Arsi zone, especially Asella area, has a conducive climate for rearing specialized dairy breeds [ 34]. The area was where the first small-scale dairy development was initiated in Ethiopia in collaboration with Swedish government [ 36]. According to the Central Statistical Agency [ 37], Arsi zone has a cattle population of 2,904,201, which is the largest from the zones of the Oromia region. The zone has 692,724 heads of cows and 154,961cross breed cows. Study design and sampling technique Lakew M, Tolosa T, Tigre W. Prevalence and major bacterial causes of bovine mastitis in Asella, South Eastern Ethiopia. Trop Anim Health Prod. 2009;41:1525–30.Liu H, Li S, Meng L, Dong L, Zhao S, Lan X, Lan X, Wang J, Zheng N. Prevalence, antimicrobial susceptibility, and molecular characterization of Staphylococcus aureus isolated from dairy herds in northern China. J Dairy Sci. 2017;100:8796–803. Da Costa LB, Rajala-Schultz PJ, Schuenemann GM. Management practices associated with presence of Staphylococcus aureus in bulk tank milk from Ohio dairy herds. J Dairy Sci. 2016;99:1364–73. http://dx.doi.org/10.3168/jds.2015-9870. Sex of farm owner, experience in dairying, education level, training on hygienic milk production, material of milk utensil and udder/teat drying were not related to TBC, CC, CPS or the presence of S. aureus in bulk milk in univariable regression analysis. Multivariable regression analysis of risk factors associated with milk quality indicators and occurrence of S. aureus in bulk milk
Ghilu S, Yilma Z, Banerjee S. Quality and marketing of milk and milk products in Ethiopia. Assessment of quality and marketing of milk and milk products in the central highland of Ethiopia. Lambert Acad Publ. 2012.
REVIEW article
Metzger S, Hernandez L, Skarlupka J, Suen G, Walker T, Ruegg P. Influence of sampling technique and bedding type on the milk microbiota: results of a pilot study. J Dairy Sci. 2018;101:6346–56. Team RC. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2020. Hamiroune M, Berber A, Boubekeur S, Smar O. Evaluation of the bacteriological quality of raw cow’s milk at various stages of the milk production chain on farms in Algeria. Rev Sci Tech Off Int Epiz. 2016;35:1–26. In recent years, the number of studies concerning microbiota of the intramammary environment has increased rapidly due to the development of high-throughput sequencing technologies that allow mapping of microbiota without culturing. This has revealed that an environment previously thought to be sterile in fact harbours a microbial community. Since this discovery, many studies have investigated the microbiota of different parts of the udder in various conditions. However, few studies have followed the changes that occur in the udder microbiota over time. In this study, the temporal dynamics of the udder microbiota of 10 cows, five with a low somatic cell count (SCC, SCC < 100,000 cells/mL) and five with a high SCC (SCC > 100,000 cells/mL), were followed over 5 months to gather insights into this knowledge gap.
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