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Review

Minimizing Bacterial Counts in Bulk Tank Milk: A Review with a Focus on Chlorine-Free Cleaning

1
Teagasc Animal and Grassland Research and Innovation Centre, Moorepark, Fermoy, P61 C996 Cork, Ireland
2
Department of Physical Sciences, Munster Technological University, Bishopstown, T12 P928 Cork, Ireland
3
Teagasc Food Research Centre, Moorepark, Fermoy, P61 C996 Cork, Ireland
*
Author to whom correspondence should be addressed.
Submission received: 19 December 2024 / Revised: 13 January 2025 / Accepted: 16 January 2025 / Published: 31 January 2025
(This article belongs to the Section Dairy Farm System and Management)

Abstract

:
The production of farm bulk milk with low bacterial counts is a key quality index used by industry to help ensure the production of high-quality dairy products. The primary metrics used to determine the microbiological quality of bulk tank milk on a farm are the total bacteria count (TBC) and thermoduric bacteria count. To maintain TBCs and thermoduric counts at the lowest attainable levels, i.e., TBC ≤ 15,000 cfu/mL and thermoduric bacteria ≤ 200 cfu/mL, it is imperative that milk quality management is treated as a multi-faceted endeavor. Milking equipment cleaning, pre-milking teat preparation, milk filtration, cooling and storage, milking equipment maintenance and management of a cow’s environment and diet must each be managed with best practice in mind if farm bulk milk is to consistently attain low TBCs and thermoduric counts. This is especially important when using chlorine-free cleaning protocols, which are more complex than traditional chlorine-based cleaning methods and if not implemented correctly do not offer the confidence of achieving required hygiene standards.

1. Introduction

Delivering milk of a high microbiological standard, i.e., a total bacteria count (TBC) of ≤15,000 cfu/mL and a thermoduric bacteria count of ≤200 cfu/mL [1], is necessary if dairy processors are to guarantee the manufacture of high-quality dairy products [2]. The total bacteria count represents aerobic bacteria (from both the environment and the mammary gland [3]) whose enzymatic activity can damage milk components, and as a result, alter end product quality [2,4]. Thermoduric bacteria, e.g., Bacillus, Clostridia and Enterococcus [5,6] originate in the environment, mainly in soil, and in contrast to bacteria that are susceptible to pasteurization, thermoduric bacteria survive the pasteurization process and persist along the manufacturing chain to the final products [7]. Producing milk with low TBCs and thermoduric counts is a multi-faceted process that requires diligent management across the entire dairy farm. Cleaning milking equipment properly [8,9,10]; maintaining cows in a hygienic state at all times, especially when milking [8,9,11]; maintaining the general farm environment, cow housing, roadways and paddock areas in a hygienic condition [12]; allocating a cow diet that is conducive to the production of high-quality milk [13,14]; cooling milk promptly post-milking and ensuring that it has been properly filtered [15,16]; and regularly servicing milking equipment [17] are all critically important if milk with low bacterial counts is to be consistently produced on a farm. Such a holistic approach is even more imperative where chlorine-free cleaning methods are used.
The use of ‘detergent sterilisers’, containing a combination of sodium hypochlorite [chlorine] and sodium hydroxide [18], have formed the basis of milking equipment cleaning regimes internationally for many years [19,20,21]. Chlorine is a key component in milking equipment cleaning protocols due to its ability to peptize proteins and eliminate a wide range of microbes, including vegetative and spore forms of bacteria as well as molds, yeasts and viruses like bacteriophages [21]. Notwithstanding this, chlorine poses a risk to milk and dairy product quality from a chemical residue perspective, i.e., chlorate, perchlorate and trichloromethane (TCM), which is also known as chloroform [20,22,23]. Chlorate and perchlorate are residues of concern due to their capacity to inhibit the normal function of the thyroid gland, particularly that of infants and young children (making these residues most pertinent to infant milk formula products) [20]. Chlorate and perchlorate are ubiquitous in chlorinated chemicals, but levels can be exacerbated over long storage periods as well as from exposure to light, heat and fluctuations in pH [20,24,25]. In contrast, TCM is a ‘possibly carcinogenic substance’ [26] that develops when chlorine and milk come in contact and it subsequently accumulates in the fat fraction of milk, making it most pertinent to high-fat dairy products such as butter [27,28]. Thus, largescale purchasers of dairy products including infant milk formula and butter have become increasingly concerned about chlorine-based residues and have set stringent maximum limits on their presence in dairy ingredients and products. In an attempt to ensure that these limits/targets are met, dairy industry stakeholders in the Republic of Ireland (ROI) took a proactive approach and made the collective decision to prohibit the use of chlorine for cleaning and disinfecting milking equipment (came into effect on 1 January 2021) [29]. This decision was the first of its kind, as the concept of cleaning without chlorine was uncommon, with the exception of some robotic milking systems [10]. Its relative novelty combined with the absence of chlorine and its efficacious biocidal and peptizing properties raised concerns as to the capacity of chlorine-free cleaning to deliver milk with low TBCs and thermoduric bacteria counts. However, Ref. [30] had previously reported seven chlorine-free cleaning protocols that were capable of effectively cleaning milking machines, over a three-month period under research conditions (Table 1).
Moreover, follow-up research conducted by [10] on commercial dairy farms in the ROI demonstrated that when chlorine-free washing protocols (selected on the basis of being the most appropriate for the particular milking parlor configuration) were implemented correctly, farm bulk milk containing low TBCs and thermoduric bacteria counts could be delivered. Moreover, in some cases TBCs/thermoduric counts achieved where chlorine-free cleaning was used were lower than those achieved on farms using chlorine-based cleaning. Further to this, TBCs and thermoduric bacteria counts from dairy farms (using chlorine-free cleaning) competing in the 2022 Irish National Dairy Council Milk Quality Awards were low, with an average TBC of 6307 cfu/mL and an average thermoduric count of 133 cfu/mL [31].
However, a study of average monthly bulk milk tank bacterial counts from farms using chlorine-free cleaning found that TBCs ranged from 15,000 cfu/mL to 45,000 cfu/mL and thermoduric counts ranged from 200 cfu/mL to 600 cfu/mL [32]. As these counts are notably higher than those reported by [10,30] during research trials and by award-winning Irish farms [31], this ultimately means that chlorine-free cleaning is being implemented on dairy farms in the ROI with varying levels of success. However, suboptimal cleaning of milking equipment is just one cause of high TBCs and thermoduric counts. Research has demonstrated that milk quality is dependent on diligent management across all areas of a farm, not just milking equipment cleaning [11]. Research has demonstrated that only 72% of Irish dairy farmers service their milking machine on an annual basis, while only 7% change milking liners every 2000 milkings [33], with just over half of farmers (52%) conducting some form of pre-milking teat preparation [12]. Research conducted in the Lombardy region in Italy reported that just under two thirds (62%) of farms were pre-dipping in advance of milking [34]. Thus, the objective of this article is to comprehensively review the range of on-farm management factors, including the application of chlorine-free cleaning protocols that are critical for the production of high microbial quality. This review of chlorine-free cleaning practices is Ireland-centric as, to the author’s knowledge, this is the only dairy industry in the world that has adopted this technology on a widespread basis. Therefore, it serves as the sole reference for dairy producers across the world.

2. Cleaning of Milking Equipment

To effectively clean milking equipment, the fundamental principles of cleaning must be adhered to, i.e., the employment of both chemical (detergents/descalers/sanitizers) and physical (turbulence) cleaning action employed in conjunction with adequate heat (hot water) and contact time (circulation time) [35]. Moreover, [36] highlighted the need for milking equipment to be cleaned after every use, e.g., after each milking for a milking machine and after each milk collection for a bulk milk tank, the purpose of which was to prevent the build-up of unwanted organic and inorganic deposits on milk contact surfaces (Figure 1). The importance of such regular cleaning is reinforced by the fact that [36] reported the necessity for such because of research conducted in the United States, a country where chlorine has maintained its position as the fulcrum of the cleaning routine to this day; this ultimately means that even the most versatile cleaning chemicals, i.e., chlorine, cannot replace regular cleaning.

2.1. Chlorine-Free Milking Equipment Cleaning Protocols

In contrast to chlorine-based cleaning protocols, which typically involve 14 chlorine-based washes per week with one additional wash using an acid descaler (phosphoric/nitric acid) when used in the Republic of Ireland, or 14 chlorine-based washes followed immediately by an acid rinse when used in the United States, or periodic chlorine-based washes (weekly/monthly) in New Zealand [21], chlorine-free cleaning is more complex and the protocols chosen depend on the type of equipment being cleaned.
Sodium hydroxide-based detergents form the basis of the majority of chlorine-free protocols. Sodium hydroxide levels in chlorine-free detergents range from 10 to 36% in liquid detergents and 50 to 74% in powder detergents [37]. In the absence of chlorine, increased levels of sodium hydroxide (relative to chlorine-based detergents) are required to achieve maximum detergency, particularly for the purpose of peptizing proteins [10,38]. Contrary to the universal chlorine-based washing protocol, there are five chlorine-free wash protocols available for milking machines (Table 2) and three for bulk milk tanks (Table 3) recommended by Teagasc, which is the food and agriculture development authority of the Republic of Ireland (https://www.teagasc.ie/media/website/animals/dairy/Chlorine-free-wash-Milk-quality-workshop2020NA.pdf) (accessed 10 October 2024).
These protocols vary depending on the type of sodium hydroxide detergent used (powder or liquid) and the number of acid washes required. In large milking plants (12 milking units or more) and/or where ancillary equipment is present, e.g., milk meters and automatic cluster removers, a routine comprising 14 hot washes per week should be employed [31] (Table 2; option 4). Where water hardness is an issue (>100 mg/L of calcium carbonate) [39], more frequent acid (phosphoric/nitric) washing is recommended, e.g., 7 acid washes and 7 caustic washes per week [31] (Table 2; option 2). Hard water occurs when there is a high dissolved mineral (magnesium/calcium/iron) content in water [40] and has been found to negatively impact bulk milk tank bacterial counts, particularly thermoduric and coliform bacteria counts [9]. The presence of hard water minerals disrupts the normal function of detergents and can also cause soiling of milk contact surfaces by way of mineral scales [41] (Figure 1).
The installation of a water softener in conjunction with regular acid washes can help reduce the disruptive properties of hard water [40]. Levels of water hardness vary with geographic region and can range from <100 mg/L of calcium carbonate (considered soft water) to 351–400 mg/L (very hard water) [39]. If the preferred unit of expression for water hardness is grains per gallon (grains/gal), as it is in some parts of the United States, this can be calculated by multiplying the mg/L figure by a conversion factor of 17.1 [40]. The geographical variation is attributed to the predominant minerals present in the bedrock of different regions, for example, limestone, which is rich in calcium, predominates in the midlands of the ROI, while sandstone (which has low levels of calcium) is the most prevalent bedrock in the southwest region with the consequence that water in the midlands tends to be hard while that from the southwest region tends to be softer [39].
‘One for All’ acid-based cleaning chemicals can be composed of nitric, glycolic, octanoic, octenylsuccinic, methanesulfonic and sulphuric acids [37]. These chemicals are specially formulated to remove both organic and inorganic deposits and can also disinfect milking equipment in a single process. It is recommended to use sodium hydroxide on at least one occasion per week when using ‘One for All’ acids to ensure that all organic deposits are removed (Table 2, option 5) [38]. ‘One for All’ chemicals have been employed to an extent in New Zealand, where regular acid washes form the basis of most wash protocols, with chlorine-based washes employed on a weekly/monthly basis [21].
Regardless of the routine employed, where a ‘dump line’ (an additional milk pipeline designated for milk that is not entering the bulk tank) is present, as on ~30% of dairy farms in the ROI [33], it must be cleaned as part of the overall wash protocol after every milking, regardless of whether it was used or not. If it is left unwashed, it can become a source of thermoduric bacteria [42].

2.2. Detergent and Acid Concentration

A critical aspect of chlorine-free washing protocols is that the correct concentrations of sodium hydroxide (detergent) and acid are used. To ensure that effective cleaning takes place, it is necessary to use the required concentrations of detergent and acid. Thus, the rate at which the sodium hydroxide detergent is diluted in wash water needs to be carefully reviewed. Where chlorine-free sodium hydroxide detergent is used in conjunction with hot water, the typical concentration required is 0.5% (v/v) of the overall solution, i.e., 500 mL of detergent in 100 L of hot water [42]. When cold water is used, an increase in solution concentration is warranted due to the absence of heat, with a typical cold wash solution containing a detergent concentration of 1% (v/v) [42]. Acid washes (hot or cold water) typically require a concentration of 1% (v/v). As specific usage rates will vary for different products, it is critical to adhere to the instructions issued by the manufacturer of each product and to note whether hot or cold water is required.

2.3. Hot Washing

Washing milking equipment with hot water is associated with low bacterial counts in bulk tank milk [8]. Using hot water in conjunction with cleaning chemicals increases the detergency of the wash solution by two- to eight-fold [43]. Previously, when chlorinated detergent sterilizers were used, a wash solution temperature of 65 °C plus at the start of the cycle was sufficient because chlorine is less volatile when used at low temperatures [44]. However, when using chlorine-free detergent (sodium hydroxide), it is necessary to have the starting temperature in the range 75–80 °C, to compensate for the absence of chlorine and in doing so maximize the detergency of the wash solution [38]. Although hot water temperature is an integral part of the wash routine, chlorine-free cleaning routines are not the most demanding in terms of hot water temperature because in some parts of the world, e.g., parts of the UK, milking equipment is cleaned using acidified boiling washes, where the acid solution enters the milking plant at 95 °C and is not circulated, but sent straight to waste [3,21].

2.4. Turbulent Flow

Milking plants with milk transfer pipes that are <50 mm in diameter will be rinsed/washed sufficiently by the ‘flood’ action of the solution flowing through the pipeline, provided the recommended volume of rinse/wash solution (14 L of water/milking unit for rinsing and 9 L of water/milking unit for washing) [1,45] is available for all surfaces of the pipe to be cleaned [46]. However, larger plants with larger milk pipelines (>50 mm in diameter) require added turbulence for effective cleaning. This is achieved by the installation of an air injection unit (situated at the end of the milk line) that retains a reservoir of water that is released as a pressurized pulse of water through the milk line every 30–40 s. These pressurized pulses of water are referred to as ‘wash slugs’ [47]. A ‘wash slug’ is essentially a ‘wave’ of water that allows all surfaces of the pipeline to be in contact with the wash solution [47]. However, the air injection system and resultant ‘wash slug’ will only create turbulence in the milk pipeline and receiver vessel. Turbulence in the claw bowl is provided via the ‘air bleed’, with the pulsation providing turbulence to clean the milking liner [46].

2.5. Wash Circulation Time

Following a post-milking rinse to remove all milk from the milking equipment, the chlorine-free detergent/acid solution should be circulated for a period of time that allows sufficient contact of the detergent/acid and the milk contact surfaces. However, circulation time must not exceed 10 min to ensure that re-adherence of previously removed deposits does not occur [1]. This is particularly important when hot water is used, as it is imperative that the temperature of the wash solution does not decrease to <45 °C at the end of the wash cycle [38].

2.6. Chlorine-Free Cleaning of the Bulk Milk Tank

Bulk milk tanks should be washed after each milk collection [36]. The typical wash cycle for a bulk tank involves a post-collection rinse to remove any milk residue, a detergent/acid cycle to clean the tank (the water volume used for the wash cycle should be equivalent to a minimum of 1% of the tank’s total capacity) and a further rinse to remove any of the detergent residue, which in some instances may be followed by an additional sanitizing rinse [38]. It is necessary to ensure that the correct volume of detergent/acid is used to clean the tank and that the internal cleaning ‘spray balls’ in place (that deliver the rinse water/wash solution to the tank surfaces) are not clogged with grit (to ensure that the wash solution reaches all of the internal tank surfaces) [48]. As outlined in Table 3, bulk tank wash protocols may include washing with acid after every second/third milk collection and with sodium hydroxide detergent after all other collections [38]. It is also possible to use sodium hydroxide detergent after each milk collection, but only in conjunction with a final rinse containing peracetic acid [38]. Using a ‘One for All’ acid product is also an option as it serves to clean, descale and in some instances sanitize the tank using a single chemical [38].

2.7. Use of Sanitizers

In the absence of chlorine, peracetic acid is the only suitable sanitizer available for use in milking machine washing routines. Peracetic acid can be used in a final rinse (all detergent must be rinsed away first) and no further rinsing is required provided it is used at the rate outlined by the manufacturer, which is typically 60 mL/45 L of water, i.e., at 0.13% (v/v). The use of peracetic acid in the final rinse was found to result in significantly lower TBC (1389 cfu/mL; p = 0.004) and numerically lower thermoduric bacteria counts (47 cfu/mL; p = 0.117) in milk relative to situations where a peracetic acid rinse was not employed (TBC: 2593 cfu/mL and thermoduric bacteria count: 75 cfu/mL) [30]. Peracetic acid is also useful for cluster disinfection during milking [38].

3. Milking-Associated Factors That Influence Bulk Milk Microbial Quality

Milk in the mammary glands of healthy cows contains very low levels of bacteria, but once extracted from the mammary gland, milk is prone to contamination from the environment [3]. However, the farmer can exert control over such contamination by adhering to good hygienic practices during the milking process, i.e., ensuring that milking clusters are attached to clean, dry teats only [49], by ensuring proper filtration, rapid cooling of the milk [15,16,50] and that milking equipment is fully functional via regular maintenance [49]. Notwithstanding the fact that these milking-related factors have been recognized for some time, they play an even more critical role in situations where chlorine-free cleaning is employed.

3.1. Pre-Milking Teat Preparation

Where a cow’s environment is particularly dirty, cow teats are likely to be significantly coated with feces and soil [48] (Figure 2). Soil is a recognized reservoir of thermoduric bacteria, thus adherence of soil to the external teat surface is associated with higher thermoduric bacterial populations in milk [51]. Due to the ubiquity of bacteria in the cow’s environment, it is best practice to clean teats before cluster attachment to minimize the bacterial load in milk, especially thermoduric bacteria [49].
There are several recommended ways of preparing cows teats for milking, e.g., dry wiping [52], using a moist disinfectant wipe [53], washing teats with water followed by drying or by applying teat disinfectant followed by drying [53]. Dry wiping with a paper towel reduced the number of thermoduric bacteria on cows’ teats by ~50%, relative to not cleaning teats at all [53]. Application of teat disinfectant as a foam and subsequently removing it with a paper towel resulted in a 91% reduction in thermoduric bacteria present on cow teats, while cleaning teats with a moist towel, followed by thorough drying, removed 96% of thermoduric bacteria present on the teats [53]. Washing teats with water followed by drying reduced the populations of Staphylococcal and Streptococcal and coliform bacteria on cow teats by 50%, 60% and 15%, respectively [54], while disinfecting teats with chlorhexidine teat foam followed by drying reduced Staphylococcal, Streptococcal and coliform bacterial populations on cow teats by 95%, 75% and 15%, respectively [54]. When teats are not prepared by a recommended methodology that includes drying of the teat after washing/disinfecting, the risk of bacteria entering milk is increased as wetting the teat surface without subsequent drying will increase the likelihood of any bacteria remaining on the surface being removed during milking and gaining access to the milk. Ref. [3] reported that when cow teats were washed with water, but not dried before milking, TBCs and coliform bacteria counts were five-fold and six-fold higher, respectively, compared to when teats were dried pre-milking. Moreover, where teat disinfectants are applied and not wiped off pre-milking, there is potential for teat disinfectant residues to contaminate milk [54,55]. Aside from enhancing milk microbiological quality, proper teat preparation also serves to reduce the risk of mastitis [3,54].

3.2. Filtering, Cooling and Storing Milk

The flow of milk through a milk filter before entering the plate cooler (where present) and the bulk milk tank helps to prevent any unwanted dirt and debris accumulated during the milking process from entering the bulk milk tank [56]. Excessively soiled milk filters may be linked to inadequate teat preparation [48] (Figure 3).
It is advised to have a clean milk filter in situ during the wash cycle, to prevent any dirt and debris released during the wash cycle from entering the plate cooler [48,57]. A properly operating plate cooler (1:2–1:3 milk:water ratio) facilitates rapid cooling of milk from its initial temperature of approximately 35 °C [50,58] to 15–17 °C, before the milk enters the bulk tank. Rapid cooling by the plate cooler (where present) and the bulk tank minimizes bacterial proliferation in stored milk [16,50]. Milk should ideally be cooled to the target storage temperature of ≤4 °C within 30 min of the end of milking [1,16]. Research has demonstrated that when good-quality milk (TBC 2512 cfu/mL before entering the bulk tank) is stored at 4 °C for 96 h, TBCs do not increase significantly (p = 0.99) during storage (TBC 4786 cfu/mL after 96 h storage) [16]. However, when storage temperature is increased to 6 °C, the TBCs of stored milk are significantly higher (p < 0.001) after 96 h storage (74,131 cfu/mL) relative to the TBCs before it enters the bulk milk tank (2692 cfu/mL) [16].

3.3. Milking Equipment Maintenance

It is recommended to service a milking machine at least once per year to ensure that it is operating satisfactorily [17]. Milking liners should also be changed every 2000 milkings or six months (whichever comes first) and long milk tubes should be changed every two years [48], whereas any worn/damaged rubberware (Figure 4) and plastic components should be changed immediately, regardless of the period between each service interval.
Cracks and crevices in worn components and rubberware accommodate bacteria as these discrete areas shield bacteria from the cleaning process and allow them to multiply within the milking system [48], e.g., Listeria monocytogenes was isolated from a milk meter with a damaged internal surface on a New York dairy farm [59]. Vacuum lines supply vacuum to the milk receiver, and even though milk does not pass through the vacuum line, it is still at risk of contamination via cracked liners/air tubes and the foaming of milk in the receiver vessel (subsequently flooding the sanitary trap with milk) [31]. Therefore, the vacuum line should be washed as part of the annual service and whenever contamination occurs.

4. Other On-Farm Factors That Influence Milk Microbial Quality

The farm environment has a significant influence on cow hygiene, regardless of whether that environment is the paddock during the grazing season or the cubicle shed in winter [60]. Akin to milking-related factors, the influence of the environment on milk microbial quality has been recognized for some time. However, where chlorine-free cleaning is used, the influence of the farm environment must be continually emphasized.

4.1. Grazing Environment

During the grazing season and particularly in wet weather, intense ‘soiling’ of cows with mud must be minimized. Measures that may be taken include the installation and maintenance of an effective farm roadway network, having multiple entry and exit points in paddocks, and strategic placing of water troughs [60,61]. Such infrastructure minimizes traffic and congregation (of the herd) in confined areas, e.g., at water troughs/gaps which would lead to surface damage, dirty teats and udders, and ultimately a large thermoduric bacterial load on cow teats [49,51,62]. Minimizing poaching (surface damage) of grazed paddocks is critically important for reducing the incidence of Bacillus cereus in bulk tank milk as poached soil increases the risk of dirty cow udders and teats [62]. It is also vital that collecting yards (areas where cows are held before and in some instances after milking) are maintained as clean as possible.

4.2. Indoor Environment

When cows are indoors, cubicle beds and cow standing areas within the shed must be cleaned regularly to prevent a build-up of feces. Moreover, an appropriate bedding material should be applied to cubicle beds to maintain them in a clean and dry condition and minimize the build-up of bacteria. Hydrated lime has been shown to be a very suitable bedding material for this purpose [15], while using sawdust or recycled manure increases the prevalence of thermoduric bacteria in the cows’ environment and ultimately in bulk tank milk, especially where teat preparation is not employed [13,14,49]. Regardless of whether cows are indoors or outdoors, their tail and udder hair must be regularly trimmed to minimize the areas (on the cow) where soils and bacteria can accumulate [49]. Trimming udder hair is associated with lower bulk tank bacterial counts and significantly increases (p = 0.01) the likelihood of having clean teat ends [8].

4.3. A Cow’s Diet

When feeding silage, either during the indoor housing period or when allocating it as a supplementary feed during the grazing season, it is vital that it is of high quality, not just from nutritional and performance points of view, but also because poor-quality silage can contain large populations of thermoduric bacteria, including Clostridium spp., Paenibacillus spp. and Bacillus spp. [51,63]. Research conducted on Swedish farms demonstrated an association between thermoduric bacterial numbers present in total mixed rations (grass silage, alfalfa silage, hay, straw, ensiled beet pulp, triticale, minerals and concentrates) and the numbers present in the feces and milk produced by cows that consumed this feed [13]. A similar trend was exhibited by Ref. [62], where milk produced by Irish dairy herds fed poor-quality silage (ensiled in wet conditions) was more likely to contain B. cereus than that from cows on a grass-only diet. When silage-containing thermoduric bacteria are eaten by a cow, the thermoduric bacteria present survive the digestion process and are subsequently excreted in the feces and deposited in the cow’s environment, e.g., standing and lying areas, and in the absence of proper teat preparation, can contaminate the milk as it is being harvested from the cow [13,14].

5. Conclusions

Achieving low bacterial counts in bulk tank milk when using chlorine-free cleaning is dependent on the consistent implementation of a recommended milking machine and bulk milk tank cleaning protocol, the fulcrum of which is adequate concentrations of detergent/acid, necessary levels of turbulence, hot water washing at the desired temperature and correct wash circulation contact time. However, other farm management factors can also contribute to bulk milk tank bacterial counts. The impact that failing to conduct recommended pre-milking teat preparation, maintain a cow’s environment in a hygienic state and feeding suboptimal quality diets can have on bulk milk bacterial counts cannot be underestimated. As consumer demand for safe and high-quality food increases, it is vital that action is taken across the entire dairy chain to ensure that these expectations are delivered. Production of milk to the highest microbial standards at the farm level is the first step towards achieving this, but without a comprehensive, cross-farm approach to the production of quality milk, this will not be attainable.

Author Contributions

L.T.—conceptualization, writing original draft, review and editing; A.F.—review and editing; B.O.—funding acquisition, administration, review and editing; T.B.—review and editing; and D.G.—funding acquisition, conceptualization, administration, review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Department of Agriculture, Food and Marine Food Institutional Research Measure (FIRM), grant number 2019R555, and by Dairy Research Ireland, project number 1163. Lorna Twomey also received the Teagasc Walsh Scholarship funded by the DAFM (FIRM) grant.

Informed Consent Statement

Ethical approval was not required as neither human nor animal subjects were involved.

Data Availability Statement

Data sharing is not applicable.

Conflicts of Interest

There are no conflicts of interest to report.

References

  1. O‘Brien, B. Bacterial Contamination. 2016. Available online: https://www.teagasc.ie/media/website/animals/dairy/Bacteria.pdf (accessed on 2 July 2024).
  2. Murphy, S.C.; Martin, N.H.; Barbano, D.M.; Wiedmann, M. Influence of raw milk quality on processed dairy products: How do raw milk quality test results relate to product quality and yield? J. Dairy Sci. 2016, 99, 10128–10149. [Google Scholar] [CrossRef]
  3. Blowey, R.W.; Edmondson, P. Mastitis Control in Dairy Herds, 2nd ed.; CAB International: Oxfordshire, UK, 2010. [Google Scholar]
  4. Paludetti, L.F.; Kelly, A.L.; Gleeson, D. Effect of thermoresistant protease of Pseudomonas fluorescens on rennet coagulation properties and proteolysis of milk. J. Dairy Sci. 2020, 103, 4043–4055. [Google Scholar] [CrossRef] [PubMed]
  5. McAuley, C.M.; Gobius, K.S.; Britz, M.L.; Craven, H.M. Heat resistance of thermoduric enterococci isolated from milk. Int. J. Food Micro. 2012, 154, 162–168. [Google Scholar] [CrossRef] [PubMed]
  6. McHugh, A.J.; Feehily, C.; Hill CCotter, P.D. Detection and enumeration of spore-forming bacteria in powdered dairy products. Front. Microbiol. 2017, 8, 109. [Google Scholar] [CrossRef] [PubMed]
  7. Doyle, C.J.; Gleeson, D.; Jordan, K.; Beresford TPRoss, R.P.; Fitzgerald, G.F.; Cotter, P.D. Anaerobic sporeformers and their significance with respect to milk and dairy products. Int. J. Food Micro. 2015, 197, 77–87. [Google Scholar] [CrossRef] [PubMed]
  8. Elmoslemany, A.M.; Keefe, G.P.; Dohoo, I.R.; Jayarao, B.M. Risk factors for bacteriological quality of bulk tank milk in Prince Edward Island dairy herds. Part 1: Overall risk factors. J. Dairy Sci. 2009, 92, 2634–2643. [Google Scholar] [CrossRef] [PubMed]
  9. Elmoslemany, A.M.; Keefe, G.P.; Dohoo, I.R.; Jayarao, B.M. Risk factors for bacteriological quality of bulk tank milk in Prince Edward Island dairy herds. Part 2: Bacteria count-specific risk factors. J. Dairy Sci. 2009, 92, 2644–2652. [Google Scholar] [CrossRef]
  10. Gleeson, D.; Paludetti, L.; O‘Brien, B.; Beresford, T. Effect of ‘chlorine-free’ cleaning of milking equipment on the microbiological quality and chlorine-related residues in bulk tank milk. Int. J. Dairy Tech. 2022, 75, 262–269. [Google Scholar] [CrossRef]
  11. Vissers, M.M.M.; Driehuis, F. On-farm hygienic milk production. In Milk Processing and Quality Management; Blackwell Publishing Ltd.: Oxford, UK, 2008; pp. 1–22. [Google Scholar]
  12. Kelly, P.T.; O‘Sullivan, K.; Berry, D.P.; More, S.J.; Meaney, W.J.; O‘Callaghan, E.J.; O‘Brien, B. Farm management factors associated with bulk tank total bacterial count in Irish dairy herds during 2006/07. Ir. Vet. J. 2009, 62, 1–7. [Google Scholar] [CrossRef] [PubMed]
  13. Magnusson, M.; Christiansson, A.; Svensson, B. Bacillus cereus spores during housing of dairy cows: Factors affecting contamination of raw milk. J. Dairy Sci. 2007, 90, 2745–2754. [Google Scholar] [CrossRef] [PubMed]
  14. Martin, N.H.; Kent, D.J.; Evanowski, R.L.; Hrobuchak, T.J.Z.; Wiedmann, M. Bacterial spore levels in bulk tank raw milk are influenced by environmental and cow hygiene factors. J. Dairy Sci. 2019, 102, 9689–9701. [Google Scholar] [CrossRef] [PubMed]
  15. Gleeson, D. Evaluation of hydrated lime as a cubicle bedding material on the microbial count on teat skin and new intramammary infection. Ir. J. Agric. Food Res. 2013, 52, 159–171. [Google Scholar]
  16. O‘Connell, A.; Ruegg, P.L.; Jordan, K.; O‘Brien, B.; Gleeson, D. The effect of storage temperature and duration on the microbial quality of bulk tank milk. J. Dairy Sci. 2016, 99, 3367–3374. [Google Scholar] [CrossRef]
  17. Fagerberg, A. Milking Machine Use and Maintenance. In Bulletin of the International Dairy Federation 418/2007; International Dairy Federation: Brussels, Belgium, 2007; p. 33. Available online: https://www.fil-idf.org/wp-content/uploads/woocommerce_uploads/2007/03/418-2007-Good-Dairy-Farming-Practices-related-to-Primary-2kr2uw.pdf#page=36 (accessed on 10 October 2024).
  18. Teagasc. Detergent Sterilisers. 2017. Available online: https://www.teagasc.ie/media/website/animals/dairy/joint-programmes/Chemicalanalysisofdetergentsterilizerproducts_201707.pdf (accessed on 28 August 2024).
  19. Gilbert, P.H. The use of detergents and sanitizers in dairy farm sanitation-an updated perspective. J. S. Afr. Vet. Ass. 1982, 53, 103–106. [Google Scholar]
  20. McCarthy, W.P.; O‘Callaghan, T.F.; Danahar, M.; Gleeson, D.; O‘Connor, C.; Fenelon, M.A.; Tobin, J.T. Chlorate and other oxychlorine contaminants within the dairy supply chain. Compr. Rev. Food Sci. Food Saf. 2018, 17, 1561–1575. [Google Scholar] [CrossRef]
  21. Reinemann, D.J.; Wolters, G.M.V.H.; Billon, P.; Lind, O.; Rasmussen, M.D. Review of Practices for Cleaning and Sanitation of Milking Machines. In Bulletin of the International Dairy Federation 418/2007; International Dairy Federation: Brussels, Belgium, 2003; pp. 3–18. Available online: https://www.oxidationtech.com/downloads/Tech/Milk%20machine%20disinfection%20practices%20non-O3.pdf (accessed on 14 September 2020).
  22. Ryan, S.; Gleeson, D.; Jordan, K.; Furey, A.; O‘Brien, B. Evaluation of trichloromethane formation from chlorine-based cleaning and disinfection agents in cow’s milk. Int. J. Dairy Tech. 2012, 65, 498–502. [Google Scholar]
  23. Ryan, S.; Gleeson, D.; Jordan, K.; Furey, A.; O‘Sullivan, K.; O‘Brien, B. Strategy for the reduction of Trichloromethane residue levels in farm bulk milk. J. Dairy Res. 2013, 80, 184–189. [Google Scholar] [CrossRef]
  24. Garcia-Villanova, R.J.; Leite, M.V.O.D.; Hierro, J.M.H.; de Castro Alfageme, S.; Hernandez, C.G. Occurrence of bromate, chlorite and chlorate in drinking waters disinfected with hypochlorite reagents: Tracing their origins. Sci. Total Environ. 2010, 408, 2616–2620. [Google Scholar] [CrossRef]
  25. Stanford, B.D.; Pisarenko, A.N.; Snyder, S.A.; Gordon, G. Perchlorate, bromate, and chlorate in hypochlorite solutions: Guidelines for utilities. J. Amer. Water Works Ass. 2011, 103, 71–83. [Google Scholar] [CrossRef]
  26. European Chemical Agency. Substance Infocard Chloroform. 2025. Available online: https://echa.europa.eu/substance-information/-/substanceinfo/100.000.603 (accessed on 12 January 2025).
  27. Fuson, R.C.; Bull, B.A. The haloform reaction. Chem. Rev. 1934, 15, 275–309. [Google Scholar] [CrossRef]
  28. Resch, P.; Guthy, K. Chloroform in milk and dairy products. Part A: Analyzis of chloroform using static headspace gaschromatography. Dtsch. Lebensm. Rundsch. 1999, 95, 418–423. [Google Scholar]
  29. Twomey, L.; Furey, A.; O‘Brien, B.; Beresford, T.; Reid, P.; Danaher MGleeson, D. Chlorate and Trichloromethane Residues in Bulk Tank Milk Produced in the Republic of Ireland before and after Chlorine was Prohibited as a Cleaning Agent on Farms. Dairy 2024, 5, 287–294. [Google Scholar] [CrossRef]
  30. Gleeson, D.; O‘Brien, B.; Jordan, K. The effect of using non-chlorine products for cleaning and sanitising milking equipment on bacterial numbers and residues in milk. Int. J. Dairy Tech. 2013, 66, 182–188. [Google Scholar] [CrossRef]
  31. Gleeson, D.; Twomey, L. Chlorine-Free Cleaning of Milking Equipment to Avoid Residues and Achieve Low Bacterial Counts in Bulk Tank Milk. 2023. Available online: https://www.teagasc.ie/media/website/animals/dairy/4.-Chlorine-free-cleaning-protocols-for-the-farm_DGleeson.pdf (accessed on 16 June 2023).
  32. O‘Brien, B. TCM, Chlorate and Microbial Status of Farm Bulk Milk—An Update. Teagasc Milk Quality Workshop 2023. 2023. Available online: https://www.teagasc.ie/media/website/animals/dairy/2.-Update-on-TCM,-chlorate-and-microbial-data-in-bulk-tank-milk_BOBrien.pdf (accessed on 1 July 2024).
  33. Uí Chearbhaill, A.; Boloña, P.S.; Ryan, E.G.; McAloon, C.I.; Burrell, A.; McAloon CGUpton, J. Survey of farm, parlour and milking management, parlour technologies, SCC control strategies and farmer demographics on Irish dairy farms. Ir. Vet. J. 2024, 77, 8. [Google Scholar] [CrossRef] [PubMed]
  34. Bava, L.; Zucali, M.; Tamburini, A.; Morandi S Brasca, M. Effect of different farming practices on lactic acid bacteria content in cow milk. Animals 2021, 11, 522. [Google Scholar] [CrossRef] [PubMed]
  35. Basso, M.; Simonato, M.; Furlanetto, R.; De Nardo, L. Study of chemical environments for washing and descaling of food processing appliances: An insight in commercial cleaning products. J. Ind. Eng. Chem. 2017, 53, 23–36. [Google Scholar] [CrossRef]
  36. Reinemann, D.; Mein, G.A.; Bray, D.R.; Reid, D.; Britt, J.S. Troubleshooting high bacteria counts in farm milk. In Proceedings of the Annual Meeting-National Mastitis Council Incorporated, Albuquerque, NM, USA, 16–19 February 1997; Volume 36, pp. 65–79. Available online: https://topmilk.msu.edu/-/media/assets/topmilk/docs/milk-money-program/part3-articles/troubleshooting-high-bacteria-counts.pdf. (accessed on 16 September 2024).
  37. Teagasc. Chemical Analysis of Chlorine-Free Detergent Cleaning Products. 2023. Available online: https://www.teagasc.ie/media/website/animals/dairy/research-farms/Chemicial-analysis-of-Chlorine-free-detergent-cleaning-products-Sept23.pdf (accessed on 16 September 2024).
  38. Gleeson, D. Moorepark Dairy Levy Research Update: Non-Chlorine Cleaning Protocols for Milking Equipment and Bulk Milk Tanks; Teagasc: Carlow, Ireland, 2018; Series 37; Available online: https://www.teagasc.ie/media/website/animals/dairy/Non-Chlorine-Cleaning-Protocol.pdf (accessed on 2 July 2024).
  39. Tedd, K.; Raymond, S.; Hunter Williams, N.H.; Kelly, C.; Lee, M.; Carey, S.; Doherty, D.; Duncan, N. Preliminary Groundwater Total Hardness Map. 2015. Available online: https://www.gsi.ie/documents/preliminary_groundwater_total_hardness_map.pdf (accessed on 24 November 2020).
  40. Watrous, G.H., Jr. Food Soils, Water Hardness, and Alkaline Cleaner Formulations. J. Milk Food Tech. 1975, 38, 163–165. [Google Scholar] [CrossRef]
  41. United States Geological Survey. Hardness of Water. 2020. Available online: https://www.usgs.gov/special-topic/water-science-school/science/hardness-water?qt-science_center_objects=0#qt-science_center_objects (accessed on 7 November 2020).
  42. Gleeson, D.; Twomey, L. Thermoduric Bacteria in Bulk Tank Milk. Irish Farm Business Dairy Magazine, Winter 2023. [Google Scholar]
  43. Watkinson, W.J. Chemistry of detergents and disinfectants. In Cleaning-in-Place: Dairy, Food and Beverage Operations.; Tamime, A., Ed.; Blackwell Publishing Ltd.: Oxford, UK, 2008; pp. 56–80. [Google Scholar]
  44. Middleton, M.S.; Panes, J.J.; Widdas, D.R.; Williams, G. Circulation cleaning of pipeline milking machines in parlours: The value of a pre-milking chlorinated rinse. Int. J. Dairy Tech. 1965, 18, 161–164. [Google Scholar] [CrossRef]
  45. O‘Brien, B. Residues in Milk. 2016. Available online: https://www.teagasc.ie/media/website/animals/dairy/ResiduesMilk.pdf (accessed on 2 July 2024).
  46. Reinemann, D.; Mein, G.A. Sizing Vacuum Pumps for Cleaning Milking Systems. In Proceedings of the Annual Meeting-National Mastitis Council Incorporated, Fort Worth, TX, USA, 20–22 February 1995; Volume 34, pp. 100–110. Available online: https://fyi.extension.wisc.edu/energy/files/2016/03/sizing-vacuum-pumps-Reinemann_Mein.pdf (accessed on 16 September 2024).
  47. Ohnstad, I. Effective cleaning of the milking machine. Livestock 2013, 18, 28–31. [Google Scholar] [CrossRef]
  48. Gleeson, D.; O‘Brien, B.; Paludetti, L. Thermodurics: Tips to Minimise Thermoduric Bacteria in Bulk Tank Milk. 2019. Available online: https://www.teagasc.ie/media/website/publications/2019/Thermodurics-tips-to-minimize-thermoduric-bacteria-in-bulk-tank-milk.pdf (accessed on 11 March 2024).
  49. Gleeson, D.; O‘Connell, A.; Jordan, K. Review of potential sources and control of thermoduric bacteria in bulk-tank milk. Ir. J. Agric. Food Res. 2013, 52, 217–227. [Google Scholar]
  50. Paludetti, L.F.; Kelly, A.L.; O‘Brien, B.; Jordan, K.; Gleeson, D. The effect of different precooling rates and cold storage on milk microbiological quality and composition. J. Dairy Sci. 2018, 101, 1921–1929. [Google Scholar] [CrossRef] [PubMed]
  51. Borreani, G.; Ferrero, F.; Nucera, D.; Casale, M.; Piano, S.; Tabacco, E. Dairy farm management practices and the risk of contamination of tank milk from Clostridium spp. and Paenibacillus spp. spores in silage, total mixed ration, dairy cow faeces, and raw milk. J. Dairy Sci. 2019, 102, 8273–8289. [Google Scholar] [CrossRef]
  52. Miller, R.A.; Kent, D.J.; Boor, K.J.; Martin NHWiedmann, M. Different management practices are associated with mesophilic and thermophilic spore levels in bulk tank raw milk. J. Dairy Sci. 2015, 98, 4338–4351. [Google Scholar] [CrossRef] [PubMed]
  53. Magnusson, M.; Christiansson, A.; Svensson, B.; Kolstrup, C. Effect of different premilking manual teat-cleaning methods on bacterial spores in milk. J. Dairy Sci. 2006, 89, 3866–3875. [Google Scholar] [CrossRef]
  54. 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, 1–7. [Google Scholar] [CrossRef] [PubMed]
  55. O‘Brien, B.; Gleeson, D.; Jordan, K. Iodine concentrations in milk. Ir. J. Agric. Food Res. 2013, 52, 209–216. [Google Scholar]
  56. Hoyle, J.B. Sediment in milk and filters for farm use. Int. J. Dairy Tech. 1977, 30, 121–126. [Google Scholar] [CrossRef]
  57. Twomey, L.; Gleeson, D. The Employment of Best Practice TBC and Thermoduric Management Strategies on Dairy Farms. Teagasc Milk Quality Workshop, January 2024. Available online: https://www.teagasc.ie/media/website/animals/dairy/The-employment-of-best-practice-TBC-and-thermoduric-management-strategies-on-dairy-farms-Teagasc-MQW-2024.pdf (accessed on 6 March 2024).
  58. Upton, J.; Murphy, M.; French, P.; Dillon, P. Dairy Farm Energy Consumption. In Proceedings of the Teagasc National Dairy Conference, Kilkenny, Ireland, 25 November 2010; pp. 87–97. [Google Scholar]
  59. Latorre, A.A.; Van Kessel, J.S.; Karns, J.S.; Zurakowski, M.J.; Pradhan, A.K.; Boor, K.J.; Jayarao, B.M.; Houser, B.A.; Daugherty, C.S.; Schukken, Y.H. Biofilm in milking equipment on a dairy farm as a potential source of bulk tank milk contamination with Listeria monocytogenes. J. Dairy Sci. 2010, 93, 2792–2802. [Google Scholar] [CrossRef] [PubMed]
  60. O‘Brien, B. Milk Quality Handbook. Practical Steps to Improve Milk Quality. 2008. Available online: https://t-stor.teagasc.ie/handle/11019/866 (accessed on 1 July 2024).
  61. Läpple, D.; Hennessy, T.; O‘donovan, M. Extended grazing: A detailed analysis of Irish dairy farms. J. Dairy Sci. 2012, 95, 188–195. [Google Scholar] [CrossRef] [PubMed]
  62. O‘Connell, A.; Ruegg, P.L.; Gleeson, D. Farm management factors associated with the Bacillus cereus count in bulk tank milk. Ir. J. Agric. Food Res. 2013, 52, 229–241. [Google Scholar]
  63. Te Giffel, M.T.; Wagendorp, A.; Herrewegh, A.; Driehuis, F.T. Bacterial spores in silage and raw milk. Antonie Van Leeuwenhoek 2002, 81, 625–630. [Google Scholar] [CrossRef] [PubMed]
Figure 1. Build-up of organic milk deposits on the internal surface of a claw bowl (left) and of inorganic mineral deposits on the internal surface of a claw bowl (right). Organic milk deposits are typically constituted of fat (butter-like substance) and protein (caramel-like substance); inorganic deposits are typically the result of hard water deposits and will appear as a tough sugar-like/white limescale-like/iron-like substance depending on the prevailing mineral in the water.
Figure 1. Build-up of organic milk deposits on the internal surface of a claw bowl (left) and of inorganic mineral deposits on the internal surface of a claw bowl (right). Organic milk deposits are typically constituted of fat (butter-like substance) and protein (caramel-like substance); inorganic deposits are typically the result of hard water deposits and will appear as a tough sugar-like/white limescale-like/iron-like substance depending on the prevailing mineral in the water.
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Figure 2. A cow with soiled teats in advance of teat preparation (left) and a cow with clean, dry teats after effective teat preparation (right).
Figure 2. A cow with soiled teats in advance of teat preparation (left) and a cow with clean, dry teats after effective teat preparation (right).
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Figure 3. An example of an excessively soiled milk filter sock (left) and a lightly soiled milk filter sock (right).
Figure 3. An example of an excessively soiled milk filter sock (left) and a lightly soiled milk filter sock (right).
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Figure 4. Examples of a cluster with a worn milk tube (left) and a cluster with a cracked air tube (right).
Figure 4. Examples of a cluster with a worn milk tube (left) and a cluster with a cracked air tube (right).
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Table 1. Total bacteria counts (TBCs) and thermoduric counts of milk where chlorine-free cleaning protocols were used to clean milking equipment.
Table 1. Total bacteria counts (TBCs) and thermoduric counts of milk where chlorine-free cleaning protocols were used to clean milking equipment.
PublicationTBCsThermoduric Counts
[30]1040–1920 cfu/mL11–44 cfu/mL
[10]2406–4172 cfu/mL20–92 cfu/mL
Total bacteria counts (TBCs) and thermoduric counts presented for [30] are those obtained from in-line milk samples, while those from [10] are those obtained from bulk tank milk samples. Both TBCs and thermoduric bacteria counts are presented as colony-forming units (cfu) per milliliter (mL) of milk.
Table 2. Five Teagasc-recommended chlorine-free wash protocols for cleaning milking machines.
Table 2. Five Teagasc-recommended chlorine-free wash protocols for cleaning milking machines.
Milking Machine Protocol* Chlorine-Free Detergent** No. Hot Washes/Week*** No. Acid Washes/Week
Option 1Powder (sodium hydroxide)32
Option 2Liquid (sodium hydroxide)77
Option 3Liquid (sodium hydroxide)43
Option 4Liquid (sodium hydroxide)142
Option 5**** Liquid (‘One For All’ acid)7/1412
* Chlorine-free detergent refers to sodium hydroxide-based detergent. ** No. of hot washes refers to the minimum number of times per week that sodium hydroxide detergent should be used in hot water (75–80 °C starting temperature). *** No. of acid washes refers to the minimum number of times per week that an acid descaler is used to wash the machine in either hot or cold water. **** The number of hot washes required when using option 5 is a minimum of 7, with any extra hot washes above this frequency being optional. An additional final rinse containing peracetic acid can be added to these five protocols as a means of sanitizing the milking machine. When cleaning a milking machine 14 L of water/milking unit is required for rinsing and 9 L of water/unit is required for washing.
Table 3. Three Teagasc recommended chlorine-free wash protocols for cleaning bulk milk tanks.
Table 3. Three Teagasc recommended chlorine-free wash protocols for cleaning bulk milk tanks.
Bulk Tank Protocol* Frequency of Acid Wash** Frequency of Detergent WashRinse with Peracetic Acid
Option 1After every second/third collectionAfter every other collectionNo
Option 2N/AAfter every collectionAfter every collection
*** Option 3After every collectionAfter every third collection (optional)No
* Frequency of acid wash refers to how often acid descalers/’One For All’ acids are used. ** Frequency of detergent wash refers to how often chlorine-free sodium hydroxide-based detergents are used. *** Option 3 pertains to the use of ‘One For All’ acids which are chemically engineered to be able to remove both organic and inorganic deposits and in the case of some products, sanitize as well. These bulk tank wash protocols are those recommended by [38].
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Twomey, L.; Furey, A.; O’Brien, B.; Beresford, T.; Gleeson, D. Minimizing Bacterial Counts in Bulk Tank Milk: A Review with a Focus on Chlorine-Free Cleaning. Dairy 2025, 6, 7. https://doi.org/10.3390/dairy6010007

AMA Style

Twomey L, Furey A, O’Brien B, Beresford T, Gleeson D. Minimizing Bacterial Counts in Bulk Tank Milk: A Review with a Focus on Chlorine-Free Cleaning. Dairy. 2025; 6(1):7. https://doi.org/10.3390/dairy6010007

Chicago/Turabian Style

Twomey, Lorna, Ambrose Furey, Bernadette O’Brien, Tom Beresford, and David Gleeson. 2025. "Minimizing Bacterial Counts in Bulk Tank Milk: A Review with a Focus on Chlorine-Free Cleaning" Dairy 6, no. 1: 7. https://doi.org/10.3390/dairy6010007

APA Style

Twomey, L., Furey, A., O’Brien, B., Beresford, T., & Gleeson, D. (2025). Minimizing Bacterial Counts in Bulk Tank Milk: A Review with a Focus on Chlorine-Free Cleaning. Dairy, 6(1), 7. https://doi.org/10.3390/dairy6010007

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