TY - JOUR
AU1 - Matte, J. J.
AU2 - Britten, M.
AU3 - Girard, C. L.
AB - Abstract Among animal products, those from ruminants are particularly rich in vitamin B12, which is naturally synthesized by the ruminal microflora and transferred to milk. Concentrations of vitamin B12 in milk vary considerably and are affected by diet. Dairy products retain, in general, a major part of the vitamin B12 naturally present in milk, some processing conditions may even add to the basal level by production of vitamin B12 from propionic bacterium in Swiss-type cheeses. Intestinal bioavailability of vitamin B12 from milk, regardless of the technological process (raw, pasteurized, or microfiltered) is greater than the synthetic form used in supplements. Vitamin B12 in Human Nutrition: Milk is a Major Source Among B vitamins, vitamin B12 occupies a very special niche. This vitamin is produced only by bacteria and archaebacteria if the cobalt supply is adequate. As opposed to other B vitamins, it is neither synthesized nor used by fungi and plants (Martens et al., 2002). Therefore, in human diets, the sole natural source of vitamin B12 comes from animal products. Among animal products, those from ruminants are particularly rich in vitamin B12, which is naturally synthesized by the ruminal microflora using cobalt as an essential precursor. After intestinal absorption in the ileum, it is stored in liver and muscles (meat) of the host or secreted in milk (Combs, 2012). In humans, vitamin B12 deficiency affects cell division and may lead to anemia and neuropathy (Combs, 2012). In the presence of vitamin B12 deficiency, increasing folic acid supply cures anemia but not neurological symptoms. In fact, by masking the hematological symptoms, folic acid could delay diagnosis of vitamin B12 deficiency until neurological damages are irreversible. Consequently, over the last decade, since folic acid fortification of flour became mandatory in many Western countries, including Canada, there has been a renewed interest for evaluation of vitamin B12 status in human populations, especially pregnant women and the elderly (Selhub et al., 2007, 2009; Selhub and Paul, 2011). In fact, a Canadian study (Ray et al., 2007) and a recent meta-analysis (Wang et al., 2012) reported that maternal dietary vitamin B12 would be the major nutrient related to neural tube defect risks in early pregnancy within populations receiving supplements of folic acid (periconceptional tablets or fortified foods). As much as 34% of all neural tube defect cases in Canada might be due to low maternal vitamin B12 status (Ray et al., 2007). Moreover, especially in the elderly population, it seems that low vitamin B12 status, even if still within the normal range, is associated with neurodegenerative disease and cognitive impairment (De Lau et al., 2009; Moore et al., 2012; Morris et al., 2012). Furthermore, cognitive decline is accelerated in individuals combining low vitamin B12 and high folate status (Morris et al., 2012). Vitamin B12 status is correlated with vitamin B12 intake in humans (Tucker et al., 2000; Vogiatzoglou et al., 2009; Bor et al., 2010). Vegetarians have lower vitamin B12 status than omnivores (Miller et al., 1991; Bor et al., 2010; Obersby et al., 2013). However, dietary sources of the vitamin also seem to matter. For example, vitamin B12 status of vegetarians was positively correlated with their intake of dairy products, especially milk, but was not correlated with egg or seafood consumption (Miller et al., 1991). Among adults not using vitamin supplements, the relationship between plasma concentration of the vitamin and its intake from dairy products is similar to the relation observed with intake of cereals fortified with vitamin B12. However, the relationship with meat, poultry, or fish intakes is weaker (Tucker et al., 2000). A Norwegian study showed that plasma concentrations of vitamin B12 increase with the amounts of vitamin B12 provided by dairy products or fish but not with those provided by eggs or meat (Vogiatzoglou et al., 2009). Moreover, for a similar intake, plasma concentrations of vitamin B12 were greater when the vitamin was supplied by dairy products compared with fish, suggesting that bioavailability of the vitamin from dairy products is greater than for other sources (Vogiatzoglou et al., 2009). Globally, these dietary surveys seem to indicate that vitamin B12 supplied by dairy products is more available than from other natural sources, although in these studies, intake data were obtained by a food-frequency questionnaire. In terms of provision of vitamin B12, one glass (250 mL) of milk provides more than 1 mg of vitamin B12 (USDA, 2011). According to the Canadian Food Inspection Agency (2010), cow milk could be labeled as an “excellent source” of vitamin B12 because one glass of milk provides nearly 50% of the recommended daily allowance (RDA; Health Canada, 2006) for adults and children over 13 years of age (2.4 mg/day). Vitamin B12 in Milk Influence of the dairy cow and its diet In 1966, Miller et al. (1966) reported that concentrations of vitamin B12 in milk were highly variable and were affected by cow breed, season, cobalt supply, and feeding regimens. These authors observed that inclusion of oat silage increased milk concentrations of vitamin B12 as compared with corn silage, but details on the studied feeding regimens or intake are scarce. More recently, in a study comparing four production systems in France, mainly characterized by their forage system (grassland or corn silage) and altitude (lowland or mountain), milk concentrations of vitamin B12 appeared to be related to the composition of the rations. Overall, increasing corn silage intake increased milk concentration of vitamin B12 (Chassaing et al., 2011). Concentrations of vitamin B12 were greater in milk of cows receiving a daily supplement of 25 mg of cobalt compared with an unsupplemented diet, but further increase of daily cobalt supply from 25 to 75 mg had no effect on milk concentrations of the vitamin (Akins et al., 2013). A study conducted on 15 commercial dairy farms in Québec, Canada, showed that vitamin B12 content in milk of cows during their first two months of lactation varied greatly among farms: from 2.0 to 3.7 ng/g, in spite of small differences in supplemental cobalt among herds (Figure 1; Duplessis et al., 2011). Recordings of calculated composition of the rations and analytical measurements were collected, but they did not allow identifying dietary factors associated with changes in milk concentrations of the vitamin. The number of farms involved was possibly too limited for such survey. Figure 1. View largeDownload slide Concentrations of vitamin B12 in milk of cows from 15 dairy herds in the province of Québec, Canada. Adapted from Duplessis et al. (2011). Figure 1. View largeDownload slide Concentrations of vitamin B12 in milk of cows from 15 dairy herds in the province of Québec, Canada. Adapted from Duplessis et al. (2011). Recently, Rutten et al. (2013) demonstrated that milk concentrations of vitamin B12 are affected by the genotype of the cow. Genomic regions associated with milk concentration of the vitamin have been identified, and this offers an interesting potential for marker-assisted genetic selection. Nevertheless, data from these few studies highlight that knowledge on factors affecting milk concentrations of vitamin B12 is very limited. It is known that vitamin B12 content in milk may be increased by 50% following weekly injections of vitamin B12 to dairy cows (Preynat et al., 2009); in such case, a glass of milk (250 mL) would provide up to 75% of the RDA. However, in commercial conditions with the variable concentrations of vitamin B12 in milk mentioned above (Duplessis et al., 2011), a glass of milk from those farms would provide from 20% to almost 40% (with an average of 33%) of the RDA. Such variations could impact the relative importance of milk and dairy products as an excellent source of the vitamin in human nutrition. Therefore, it is important to identify the factors affecting milk concentrations of vitamin B12 and to develop sustainable nutritional strategies to promote microbial synthesis of this vitamin in the rumen of the cow and its transfer to milk. Based on the new findings of Rutten et al. (2013) described previously, genetic selection can also be a way to increase vitamin B12 in cow milk. View largeDownload slide With the permission of M. Duplessis. View largeDownload slide With the permission of M. Duplessis. Effect of processing Raw milk is industrially processed into a wide range of dairy products. Heating, mechanical or membrane separation, and fermentation are among the treatments that could potentially alter vitamin B12. Concentrations of vitamin B12 in dairy products range from a low of 1.4 ng/g in butter to more than 30 ng/g in some cheese varieties (USDA, 2011). Vitamin B12 was shown to resist pasteurization (75°C for 16 seconds), and it remains stable during storage of pasteurized milk in a domestic refrigerator for nine days (Andersson and Öste, 1994). It is also resistant to the intense heating treatment (95°C for 5 minutes) applied to milk before fermentation for yogurt production (Arkbåge et al., 2003). Appreciable loss (30 to 40%) of vitamin B12 was, however, observed in milk after boiling for 30 minutes or microwave heating for 5 minutes (Watanabe et al., 1998). Compared with pasteurized milk, vitamin B12 content in canned evaporated milk is reduced by as much as 65%, despite the concentration factor due to evaporation (USDA, 2011). Adenosylcobalamin, a predominant form of vitamin B12 in milk, is known to be sensitive to light, and Watanabe et al. (2000, 2013) suggested that cobalamin concentration in milk could be reduced by light exposure. However, no decrease in vitamin B12 concentration could be detected in milk after exposure to daylight (Scott et al., 1984) or fluorescent light (Saffert et al., 2006). Fermentation of heat-treated milk to produce yogurt results in a 25% loss of vitamin B12 content (Arkbåge et al., 2003). A further decrease (26%) in vitamin B12 concentration was observed during storage of yogurt at 4°C for 14 days. It has been suggested that the starter culture used for milk fermentation consumed vitamin B12 and was responsible for these substantial losses (Arkbåge et al., 2003). However, a similar decrease in vitamin B12 concentration was observed during the storage of non-fermented milk acidified with a mixture of lactic, acetic, and citric acids (Reddy et al., 1976). This result suggests that the stability of vitamin B12 in acidified milk might be impaired by low pH or chelating properties of organic acids. Vitamin B12 concentration in cheese varies from 2.8 ng/g in cream cheese to 8.5 ng/g in cheddar, 22.9 ng/g in mozzarella, and 33.5 ng/g in Swiss-type cheese (USDA, 2011). Vitamin B12 is water soluble, and its theoretical concentration in cheese should be less than that of milk and proportional to moisture content. However, because vitamin B12 in milk is bound to milk proteins, including caseins (Gizis et al., 1965), it is partially retained in cheese curd. In hard cheeses, the retention of vitamin B12 is around 50% (Arkbåge et al., 2003). As for yogurt, cheese storage is likely to influence vitamin B12 concentration due to starter and adjunct cultures consuming vitamin B12 during ageing. This factor could explain why vitamin B12 content is 2.7 times greater in mozzarella than in cheddar cheese. Mozzarella cheese is consumed a few weeks after production, and the bacterial activity is reduced by cooking and stretching the curd in hot water, while bacterial activity in cheddar cheese is maintained during a long ripening period (up to a few years). Despite a longer ripening period, Swiss-type cheese contains 45% more vitamin B12 than mozzarella cheese, which is attributed to the production of vitamin B12 by propionic bacterium during ripening (Gardner and Champagne, 2005). Propionibacteria are used as an adjunct culture for manufacture of Swiss-type cheeses where they are responsible for the characteristic flavor and eye formation (Poonam et al., 2012). In summary, dairy products are good sources of vitamin B12 and could be even better sources by using milk with naturally increased vitamin concentration and adapting processing conditions to maximize vitamin retention. View largeDownload slide Thinkstock/Tom England View largeDownload slide Thinkstock/Tom England The advantage of natural source In addition to the absolute amount of vitamin B12 present in milk, its availability for intestinal absorption is also an important factor for assessing the quality of this source of vitamin B12 for humans. Cyanocobalamin is the synthetic form of vitamin B12 present in most supplements, the cyanide group being used to stabilize the cobalamin molecule. However, cyanocobalamin is not biologically active until the cyanide group is enzymatically removed (Herbert, 1988). Bioavailability of the synthetic form of vitamin B12 is inversely dependent on the amount given, being less than 4% in humans and animals receiving prophylactic or therapeutic levels of supplements (Le Grusse and Watier, 1993; Scott, 1997; Matte et al., 2010). In milk, vitamin B12 is present as adenosyl-, hydroxo-, and methylcobalamin (Farquharson and Adams, 1976; Fie et al., 1994). Adenosylcobalamin and methylcobalamin have a coenzymatic activity in mammal cells and are biologically active whereas hydroxocobalamin is the product of their photolysis. In a recent experiment (Matte et al., 2012), it was hypothesized that the important daily provision of vitamin B12 brought by unprocessed (raw) or processed milk (pasteurized or micro-filtered) is more efficiently absorbed than the synthetic form (cyanocobalamin) used in vitamin supplements. Using pigs as an animal model for humans, this study compared the net portal flux of vitamin B12 (an indicator of intestinal absorption) after ingestion of milk (raw, pasteurized, or microfiltrated) to the equivalent amount of cyanocobalamin or to a control diet devoid of vitamin B12. The efficiency of intestinal absorption of vitamin B12 in milk is close to 10% regardless of the technological process (raw, pasteurized, or microfiltered) while the net flux of this vitamin to the portal vein was undetectable after ingestion of a synthetic supplement of vitamin B12 or a control meal without vitamin B12 (Table 1). Table 1. Intestinal absorption of vitamin B12 in the portal vein of pigs over 24 hours according to sources of vitamin B12.* View Large Table 1. Intestinal absorption of vitamin B12 in the portal vein of pigs over 24 hours according to sources of vitamin B12.* View Large Two hypotheses were suggested by Matte et al. (2012) to explain the greater bioavailability of vitamin B12 naturally present in milk. One was related to the molecular form of this vitamin in milk, mostly adenosylcobalamin (Farquharson and Adams, 1976; Fie et al., 1994) as mentioned previously. Information on the relative intestinal availability of the different forms of cobalamin is scarce. The only data available compared whole-body retention of crystalline radioactive forms of different cobalamins in human subjects (Weissberg and Glass, 1966; Adams et al., 1971). At doses between 100 and 1000 mg, there was no difference between cyanocobalamin and hydroxocobalamin (Weissberg and Glass, 1966). At 25 mg, whole-body retention of vitamin B12 was greater after ingestion of crystalline forms of adenosyl-, hydroxo-, and methylcobalamin than cyanocobalamin (Adams et al., 1971). Another explanation for the increased bioavailability of milk vitamin B12 was related to the presence of specific components in milk facilitating its absorption. In pigs, Matte et al. (2010) reported measurable intestinal absorption of vitamin B12 after ingestion of cyanocobalamin supplements given in a semi-purified diet, containing 16% of vitamin-free casein (derived from cow milk) whereas Matte et al. (2012) did not detect any absorption when cyanocobalamin supplements were mixed with cereals. This finding supports the hypothesis that a milk component, not destroyed by the technological process for production of vitamin-free casein, improves intestinal absorption of vitamin B12. In fact, casein itself could be involved because fractions of this protein were identified as major components of the protein binding capacity of vitamin B12 in bovine milk (Gizis et al., 1965). According to preliminary data from a study evaluating methods to increase intestinal absorption of a bolus of cyanocobalamin infused in the abomasum of dairy cows, absorption of vitamin B12 in the small intestine was greater when cyanocobalamin was given in combination with casein than when given alone (Artegoitia et al., 2013). Food proteins are known to bind vitamin B12 and affect its stability and bioavailability (Herbert, 1988; Neale, 1990). The binding proteins in milk are likely to influence acid tolerance and release of vitamin B12 at gastric pH, providing an adequate protection and release during gastric transit. Globally, these explanations are in accordance with the numerically greater, although not statistically significant, efficiency of absorption of dietary 58Co-labeled cyanocobalamin when given in milk (65%) rather than in water or bread (55%; Russell et al., 2001). Moreover, fortified breakfast cereal showed a stronger impact on vitamin B12 status than meat (Tucker et al., 2000). Since breakfast cereal is usually consumed with milk, proteins from milk might be responsible for increased bioavailability. In fact, it appears that milk and dairy products could be efficient carriers for both endo- and exogenous vitamin B12. Further information on the effect of milk-specific components on absorption of vitamin B12 is needed to understand if and how the different milk products (e.g., cheese and yogurt) derived from different fractions of milk retain the original properties of milk in terms of bioavailability of vitamin B12. View largeDownload slide Thinkstock/moodboard View largeDownload slide Thinkstock/moodboard Conclusion The presence of vitamin B12 in cow milk has a considerable impact for the overall worldwide provision of this vitamin for humankind. This is all the more important that all plant food sources are devoid of this vitamin. This provision of vitamin B12 from milk is important not only in terms of quantity, as an animal product from ruminants, but also in terms of quality, milk vitamin B12 being more bioavailable than its synthetic form currently available in nutraceutical or pharmaceutical markets. Dietary surveys in human populations showing that vitamin B12 status is highly correlated with dairy product intake indicate that consumption of cow milk could become a natural prophylactic tool and then a unique alternative to mandatory fortification of some foods to prevent vitamin B12 deficiencies in human nutrition. J. Jacques Matte is a research scientist for Agriculture and Agri-Food Canada at Sherbrooke in Québec. He obtained his Ph.D. at Université Laval, QC, Canada in 1984, was a post-doc in the UK in 1985, and had a sabbatical year in France in 1994. He is currently adjunct professor at Université Laval and at University of Alberta, AB, Canada. For the last three years, he was Associate Editor in the non-ruminant section of Journal of Animal Science. His main research areas are related to metabolism of vitamins and trace minerals and their impact for growth and for male and female reproduction in pigs. Michel Britten has been a senior research scientist at the Food Research and Development Centre, Agriculture and Agri-Food Canada, at St-Hyacinthe, Québec, Canada since 1987. He is also an adjunct professor at Laval University (Food Science and Nutrition Department) and a member of the Dairy Science and Technology Centre (STELA) and the Institute of Nutrition and Functional Foods (INAF). His main research area relates to the physical chemistry of milk and dairy products. Recent activities covered the following topics: 1) development of nutritionally enhanced dairy products, 2) nutrient protection during gastrointestinal transit, and 3) production of value-added ingredients derived from cheese whey. Christiane L. Girard has been a research scientist at the Dairy and Swine Research and Development Centre, Agriculture and Agri-Food Canada, at Sherbrooke, Québec, Canada since 1985. 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Google Scholar CrossRef Search ADS PubMed  © 2014 Matte, Britten, and Girard This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial reuse, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
TI - The importance of milk as a source of vitamin B12 for human nutrition
JF - Animal Frontiers
DO - 10.2527/af.2014-0012
DA - 2014-04-01
UR - https://www.deepdyve.com/lp/oxford-university-press/the-importance-of-milk-as-a-source-of-vitamin-b12-for-human-nutrition-UXAu0BwblQ
SP - 32
EP - 37
VL - 4
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DP - DeepDyve
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