The main steps of operation are: 1: Sanitizing; 2: Conditioning; 3: Heat processing and cooling. The inlet temperature in the heating section either hot water in steps 1 and 2, raw DHM in step 3, or water or cleansing solutions in steps 4—8 is shown in yellow; the temperature of the fluid at the exit of the holding tube is shown in red; and, the temperature of the fluid at the exit of the cooling section is shown in blue.
The gray line at the bottom represents the fluid flow. The cleaning procedure comprises four steps after each processing. The effectiveness of the thermal sanitizing step was checked for each processing cycle by microbiological analysis.
Identification of the isolates obtained in the different growth media revealed their poor selectivity since some bacterial species could be isolated from up to three different growth media e.
Figure 4. Microbiological counts in raw DHM. The number of different microorganisms in a same raw DHM production batch ranged from 3 to 10, although seven was the most frequent number Supplementary Table 2.
In relation to Gram-positive bacteria, S. Table 1. Microbiological characterization of the 14 batches of raw DHM analyzed in this study. The variety of Gram-negative bacteria identified was wider than that of Gram-positive ones and, globally, included isolates belonging to eight genera Table 1 , Supplementary Table 2. Although the frequency of detection of some species of Pseudomonas and Stenotrophomonas in raw DHM was lower, such bacteria reached the highest levels 5.
Yeasts were scarcely isolated Table 1. Survivors were detected only in five production batches and were identified as B. Table 2. The analysis of PFGE profiles of the enterococci isolated from DHM samples before and after different heat treatments revealed the existence of, at least, four pulsotypes that were closely associated to specific production batches Figure 5. In fact, as an example, the same pulsotype was shared by E.
Isolates from different batches did not share the same PGFE profile, except for two production batches L4 and L9 where the same profile was shared by all nine isolates. Figure 5. In all of these cases, B. All hot water samples collected at the end of the sanitation step, and prior the processing of a DHM production batch, over the course of this study were seeded on BHI agar for microbiological analysis.
Bacterial growth was not observed in any sample. Figure 6. Figure 7. Furosine was detected in all DHM samples analyzed, both before and after any of the applied heat treatments, and its content is presented in Table 3.
Holder pasteurization of DHM increased significantly the concentration of furosine mean value of 4. Table 3. The heat exchangers were designed and constructed in order to have a self-draining design and a small dead volume about mL , thereby minimizing DHM losses. In addition, the heat treatment is independent of packaging, allowing packing pasteurized DHM in accordance with the needs and preferences of the HMB. CIP cleaning and sanitation of the whole HTST system before operation without dismantling the equipment and without direct manipulation of chemical products contributes to enhance safety and DHM quality.
There has been some controversy regarding the use of raw or pasteurized DHM. On the other hand, DHM is a vehicle for potentially pathogenic microorganisms and, as a consequence, most HMBs consider that DHM must be processed in order to guarantee its microbiological safety. In spite of undesirable changes related to heat treatment, pasteurized DHM still retains some beneficial and protective effects, and it is preferred to infant formula Quigley and McGuire, ; Sisk et al.
Unfortunately, the pasteurizers commercially available at present are very limited regarding the retention of some bioactive components and the amount of milk that can be processed between 4 and 10 L per batch Underwood, Bacteria could be isolated from all the raw human milk batches in the different culture media employed in this study.
The high concentrations of enterobacteria, Pseudomonas spp. Contaminating bacteria, arising from environment or rinsing water Cervia et al. In dairy industry pasteurization is designed to achieve at least a five-log reduction or Spore-forming bacteria, on the other hand, can survive milk pasteurization Sarkar, The purpose of pasteurization is making DHM safe for consumption, and this requires destroying all common pathogens O'Connor et al.
However, the most thermoresistant non-sporulated microorganism has not been defined in DHM. On the other hand, as the microbiological quality of pasteurized DHM depends on the initial microbiota present in raw DHM, the specific processing conditions applied, and the storage conditions, donors should receive a good education on hygienic milk extraction and storage from the HMB staff.
In order to reach the pasteurization objective, this process should be implemented to heat the milk homogeneously, at a consistent temperature and for the correct time.
Only two bacterial species B. Holder pasteurization kills commensal and contaminant vegetative bacterial cells found in DHM but spore-forming bacteria, such as B. Subsequently, such bacteria can grow in heat-treated milk even faster than in raw milk because of the heat damage to the milk bacteriostatic systems and the absence of competitors Ford et al.
In agreement with our results, B. Additionally, it has been found in milk of healthy rhesus monkeys Jin et al. Although any milk bottle with a culture-positive result after pasteurization is rejected by most HMBs, a previous study revealed that all B.
However, as the level of virulence is highly variable among different strains Decousser et al. Refrigeration or freezing of pasteurized DHM should be strictly applied to control the growth of any remaining microorganism.
Although a relative high number of B. Despite E. Therefore, the later treatments were efficient in killing any vegetative cell initially present in raw human milk samples. Enterococci, and particularly E. During and shortly after birth, newborn infants are colonized with enterococci Moles et al. However, E. Therefore, raw DHM should receive a heat treatment compatible with the complete killing of these enterococcal species.
Molecular analysis of enterococci isolated before and after the heat treatment showed a variety of strains present in raw DHM. The thermotolerance of E. The heat resistance 60— Similarly, Silva Laport et al. Silva Laport et al. Globally, it means that the conditions for routine pasteurization of DHM must be chosen very carefully after a tough validation process, such as the described in the present study.
Alkaline phosphatase ALP is a membrane—bound glycoprotein that is found in most human tissues and is relevant in clinical chemistry as it serves as indicator of physiological functions and certain diseases. The role of milk ALP in health and nutrition of the newborn infant is uncertain Bjelakovic et al. However, it has been used traditionally in dairy industry for the evaluation of milk pasteurization processes due to the close relationship between its thermal resistance and the different time-temperatures treatments required for effective pasteurization Kay and Graham, The main advantage is that the result would be available in a short time allowing taking preliminary decisions about the processed batch in the HMB.
The usefulness of an enzyme indicator depends not only on the amount of the enzyme present in the milk and the sensitivity of the enzymatic assay, but also on the decimal reductions required for the microbial targets. In dairy industry it has been known for long time that ALP reactivates under certain conditions and alternative indigenous enzymes have been proposed.
GGTP, another glycoprotein associated to mammalian tissue and found both in the skim milk fraction and in the milk fat globule membrane, has been the most promising alternative Fox and Kelly, The activities of both enzymes, ALP and GGTP, can be assayed using simple colorimetric methods and, therefore, could be used as quick, simple, and inexpensive tests.
However, additional experiments are needed to confirm its inactivation kinetics before its potential can be exploited. Heat treatment of milk triggers different chemical reactions involving lactose such as the Maillard reaction, after reaction with proteins, and isomerization. The extent of both reactions depends strongly on the processing conditions Olano et al. Lactulose, which is mainly formed by isomerization of lactose, is not present naturally in raw DHM and was not detected in any HTST treated DHM samples in this work, however lactulose was quantified in the HoP DHM samples at similar levels to those found in samples of human milk and colostrum pasteurized by Holder method in other studies Lactulose was quantified in commercial HTST pasteurized cow's milk and values ranged from This could be explained by higher intensity of the heat treatments applied in the dairy industry.
Previously it was reported that this disaccharide, quantified by using an enzymatic-spectrophotometric method, could be used as a process indicator for commercially pasteurized and direct UHT-treated cow milk samples Marconi et al. On the other hand, Maillard reaction is one of the main reactions causing deterioration of proteins during processing and storage of foods. This reaction can promote nutritional changes such as loss of nutritional quality by destruction of essential amino acids, reduction of protein digestibility and amino acid availability.
Furosine is used as an indicator of early stages of Maillard reaction and is considered a useful indicator of the damage in processed foods or foods stored for long periods of time Corzo-Martinez et al. Taken together, the absence of lactulose and the low amount of furosine found in HTST-treated DHM strongly indicate that this heat-treatment does not induce significant heat damage in DHM.
In addition, the processing time and labor force, and therefore operational costs, should be reduced significantly in comparison with regular Holder pasteurization. Immunological, biochemical and nutritional quality of DHM processed by this new HTST equipment is currently been analyzed in order to evaluate its impact on a large number of compounds with biological activity and nutrient content and compare it to HoP DHM.
Therefore, this HTST system will provide efficiently high quality safe pasteurized DHM to preterm and sick infants admitted in most neonatal units. DE-V participated in the design of the study, acquisition of the samples, carried out the pasteurization processes, performed the microbiological and enzymatic assays, analyzed and interpreted the data, and drafted the manuscript.
IE-M participated in the design of the study and in the data analysis. JR designed the study and provided critical revisions of the manuscript for important intellectual content. NC and AM conducted the lactulose and furosine assays and participated in the data analysis. CP-A and LF participated in the design of the study, funding acquisition, analysis of the data and provided a critical revision of the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Department of Health and Human Services. Public Health Service. Food and Drug Administration World Health Organization Requisite scientific parameters for establishing the equivalence of alternative methods of pasteurization. Almutawif, Y. A retrospective audit of bacterial culture results of donated human milk in Perth, Western Australia.
Early Hum. Ballard, O. Human milk composition: nutrients and bioactive factors. North Am. Baro, C. Effect of two pasteurization methods on the protein content of human milk.
Becker, G. Methods of milk expression for lactating women. Cochrane Database Syst Rev. Berthold-Pluta, A. The effect of selected factors on the survival of Bacillus cereus in the human gastrointestinal tract. Bjelakovic, L. Alkaline phosphatase activity in human milk during the first month of lactation. Acta Facultatis Medicae Naissensis. Of course, pasteurization is in the news these days because of the debate about raw milk.
The market is growing of consumers seeking unprocessed foods or those wanting to support small farms. And advocates of raw milk defend it for a number of reasons, particularly arguing that pasteurization reduces the nutritional and health benefits of milk. But, without pasteurization, E. According to the Centers for Disease Control and Prevention CDC , there were outbreaks due to consumption of raw milk or raw milk products reported between and Bacteria not only causes milk to sour but certain types of bacteria also cause illness, so minimizing bacteria in milk is important.
Drinking ONLY pasteurized milk from an approved source is the only way of ensuring the safety of your milk and protecting you and your family. Request an amendment to a birth certificate? Check restaurant inspections? Apply for WIC? Get Help to Quit Smoking? Check out home health service providers? Report a foodborne illness? File a complaint about a health care facility? How can milk become contaminated?
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